Tuberculosis - Eurosurveillance

E u r o p e ’ s j o u r n a l o n i n f e c t i o u s d i s e a s e e p i d e m i o l o g y, p r e v e n t i o n a n d c o n t r o l 

Special Focus: 

Tuberculosis 

March 2010 

Tuberculosis (TB) continues to be a health threat to European 

citizens. This is due to the diverse epidemiological situation 

of tuberculosis burden in EU Member States with high rates of 

tuberculosis in vulnerable populations. Moreover, multi-drug 

resistance and now extensively drug-resistant (XDR TB) are a 

standing threat to tuberculosis control. Eurosurveillance reports 

on the resistance problem and analyses treatment outcomes in 

the European Union and European Economic area. 

www.eurosurveillance.org 

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Scientific Editors 

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Assistant Editors 

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Associate Editors 

Andrea Ammon, ECDC, Stockholm, Sweden 

Tommi Asikainen, ECDC, Stockholm, Sweden 

Mike Catchpole, Health Protection Agency, 

London, United Kingdom 

Denis Coulombier, ECDC, Stockholm, Sweden 

Christian Drosten, Universitätsklinikum Bonn, Bonn, Germany 

Johan Giesecke, ECDC, Stockholm, Sweden 

Herman Goossens, Universiteit Antwerpen, Antwerp, Belgium 

David Heymann, World Health Organisation, Geneva, 

Switzerland 

Irena Klavs, National Institute of Public Health, Ljubljana, 

Slovenia 

Karl Kristinsson, Landspitali University Hospital, Reykjavik, 

Iceland 

Daniel Lévy-Bruhl, Institut de Veille Sanitaire, Paris, France 

Richard Pebody, Health Protection Agency, London, 

United Kingdom 

Panayotis T. Tassios, University of Athens, Athens, Greece 

Hélène Therre, Institut de Veille Sanitaire, Paris, France 

Henriette de Valk, Institut de Veille Sanitaire, Paris, France 

Sylvie van der Werf, Institut Pasteur, Paris, France 

Design / Layout 

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© Eurosurveillance, 2010 

Austria: Reinhild Strauss, Vienna 

Belgium: Koen De Schrijver, Antwerp 

Belgium: Sophie Quoilin, Brussels 

Bulgaria: Mira Kojouharova, Sofia 

Croatia: Borislav Aleraj, Zagreb 

Cyprus: Olga Poyiadji-Kalakouta, Nicosia 

Czech Republic: Bohumir Križ, Prague 

Denmark: Peter Henrik Andersen, Copenhagen 

England and Wales: Neil Hough, London 

Estonia: Kuulo Kutsar, Tallinn 

Finland: Hanna Nohynek, Helsinki 

France: Judith Benrekassa, Paris 

Germany: Jamela Seedat, Berlin 

Greece: Rengina Vorou, Athens 

Hungary: Ágnes Csohán, Budapest 

Iceland: Haraldur Briem, Reykjavik 

Ireland: Lelia Thornton, Dublin 

Italy: Paola De Castro, Rome 

Latvia: Jurijs Perevoščikovs, Riga 

Lithuania: Milda Zygutiene, Vilnius 

Luxembourg: Robert Hemmer, Luxembourg 

FYR of Macedonia: Elisaveta Stikova, Skopje 

Malta: Tanya Melillo Fenech, Valletta 

Netherlands: Paul Bijkerk, Bilthoven 

Norway: Hilde Klovstad, Oslo 

Poland: Malgorzata Sadkowska-Todys, Warsaw 

Portugal: Judite Catarino, Lisbon 

Romania: Daniela Pitigoi, Bucharest 

Scotland: Norman Macdonald, Glasgow 

Slovakia: Lukáš Murajda, Bratislava 

Slovenia: Alenka Kraigher, Ljubljana 

Spain: Elena Rodríguez Valín, Madrid 

Sweden: Aase Sten, Stockholm 

Turkey: Aysegul Gozalan, Istanbul 

European Commission: Paolo Guglielmetti, Luxembourg 

World Health Organization Regional Office for Europe: Nedret 

Emiroglu, Copenhagen

Contents 

Special issue: Tuberculosis 

Editorials 

Improving tuberculosis surveillance in Europe is 

key to controlling the disease 2 

L D’Ambrosio, R Centis, A Spanevello, GB Migliori 

Rapid communications 

Multidrug- and extensively drug-resistant 

tuberculosis: a persistent problem in the 

European Union and European Economic Area 4 

C Ködmön, V Hollo, E Huitric, A Amato-Gauci, D Manissero 

Surveillance and outbreak reports 

Surveillance of extensively drug-resistant 

tuberculosis in Europe, 2003-2007 9 

I Devaux, D Manissero, K Fernandez de la Hoz, K Kremer, D 

van Soolingen, on behalf of the EuroTB network 

Analysis of tuberculosis treatment outcomes in the 

European Union and European Economic Area: 

efforts needed towards optimal case management 

and control 15 

D Manissero, V Hollo, E Huitric, C Ködmön, A Amato-Gauci 

Risk of developing tuberculosis from a school 

contact: retrospective cohort study, United 

Kingdom, 2009 24 

M Caley, T Fowler, S Welch, A Wood 


Coloured scanning electron micrograph (SEM) of the phagocytosis of Mycobacterium bovis (Bacillus 

Calmette-Guerin strain (BCG) used for vaccination, in red) by a macrophage white blood cell. Magnification: 

x2,900 when printed 10 centimetres wide. 

© Science Photo Library 

1

Editorials 

Improving tuberculosis surveillance in Europe is key to 

controlling the disease 

L D’Ambrosio 1 , R Centis 1 , A Spanevello 1,2 , G B Migliori 1 

1. WHO Collaborating Centre for TB and Lung Diseases, Fondazione S. Maugeri, Care and Research Institute, Tradate, Italy 

2. Universita` degli Studi dell’Insubria, Varese, Italy 

Citation style for this article: 

D’Ambrosio L, Centis R, Spanevello A, Migliori GB. Improving tuberculosis surveillance in Europe is key to controlling the disease. Euro Surveill. 

2010;15(11):pii=19513. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19513 

DNA of Tuberculosis (TB) bacteria were found in mammoth 

bones and in Egyptian mummies and TB has 

affected mankind since its appearance, despite many 

efforts to control and eliminate it [1]. 

It was already well known since the sanatoria period 

(Germany, 1857) when treatment against TB consisted 

of good food, rest, sun, and fresh air that about half 

of TB cases recovered almost spontaneously. Robert 

Koch’s discovery of Mycobacterium tuberculosis in 

1882, Carlo Forlanini introduced the artificial pneumothorax 

in 1907 [1] and streptomycin was introduced at 

the end of the Second World War. These discoveries 

revolutionised the understanding and treatment of TB. 

In spite of these discoveries, the epidemic trend has 

tended more towards an increase in recent years. The 

interventions recommended by the directly observed 

treatment, short-course (DOTS) and the Stop TB 

Strategy introduced in 2006 [2], e.g. rapid diagnosis 

of 70% of existing sputum smear-positive cases and 

effective treatment of 85% of them, are very powerful 

in reversing the epidemic trend. This was demonstrated 

in several countries, e.g. in Peru and recently 

in Europe: Romania achieved 70/85% targets and, after 

an initial increase, was able to reduce both its case and 

case-fatality load [3]. 

Multidrug-resistant (MDR) and extensively drug-resistant 

(XDR) TB mainly emerge as the result of mis management 

of TB, either by the prescribing physician 

(regimen, dose, duration) or the patient (compliance). 

Failure of the programme contributes as well: poor 

quality drugs, lack of public health action in ensuring 

patient support and correcting early signs of sub-optimal 

patient management represented by late sputum 

smear and culture conversion, presence of failures, 

defaulters and avoidable deaths. 

As underlined by the joint ECDC and World Health 

Organization Regional Office for Europe TB report, 

launched on 18 March [11] the importance of good surveillance 

to stem this trend cannot be underestimated. 

Article published on 18 March 2010 

Where do we go with surveillance in Europe? Can we do 

more? How many MDR and XDR TB cases occur because 

of sub-optimal patient management? 

This issue of Eurosurveillance casts light on these 

important questions with four interesting articles [4-7]. 

A paper by Manissero et al. from the ECDC reports on surveillance 

data in twenty-two countries of the European 

Union (EU) and European Economic Area (EEA) done by 

the ECDC Tuberculosis Programme [4]. Treatment outcome 

monitoring was performed on culture-confirmed 

pulmonary TB cases reported in 2007. While the overall 

treatment success rate was 73.8% (79.5% among new 

cases), only three countries achieved the 85% success 

rate target as a result of high defaulting and a relevant 

proportion of unknown outcomes. 

A surveillance report by Devaux et al. [5] describes retrospectively 

the results of second-line drug susceptibility 

testing (DST) among MDR TB cases reported in 

20 countries of the WHO European Region (15 being 

EU countries) aimed at identifying XDR TB. In 18 countries 

(only) DST was performed for two or more of the 

second-line drugs defining XDR TB, with relevant intercountry 

variation on the proportion of isolated tested. 

Overall, 10% of the MDR TB strains are found to be XDR. 

A report by Ködmön et al. [6] describes the surveillance 

data collected by ECDC from EU and EEA countries. In 

2008, the combined proportion of new and retreated 

MDR TB cases was 6.0% of the total case load for the 25 

countries reporting data. Thirteen countries provided 

data on resistance to second-line drugs, allowing the 

identification of XDR TB cases. 68 XDR TB cases were 

reported in 2007 (6.1% of the MDR TB cases) and 90 in 

2008 (7.3% of the MDR TB cases). Latvia and Romania 

notified the highest number of XDR TB cases in 2008. 

Next is a surveillance report by Caley et al. on a retrospective 

cohort study performed in the UK to quantify 

the risk of developing TB infection or disease following 

school contact with an infectious student. The report 

results suggest that greater levels of classroom 

2 www.eurosurveillance.org

contact with a sputum smear positive student significantly 

increases the risk of contracting both active TB 

disease and latent TB infection. 

The results of the studies reported in this issue of 

Eurosurveillance allow us to point out some key topics: 

• The completeness of reporting information (including 

treatment outcomes), the proportion of culture-confirmed 

TB cases reported as well as the 

proportion of strains on which DST for both first- 

and second-line drugs is performed and reported 

are still sub-optimal overall in Europe. The relevance 

of these pitfalls goes beyond the “simple” 

surveillance limitation, having the potential to 

affect other important TB control pillars, e.g. infection 

control and case-management. 

• MDR and XDR TB still persist in Europe. The high 

proportion of MDR TB identified among new TB 

cases reported by certain countries indicates that 

sub-optimal infection control practices are likely 

to occur, while the high percentage of MDR TB 

notified among retreatment cases is probably the 

result of sub-optimal case management in the past 

decade. 

ECDC is managing surveillance of TB at the EU level 

in collaboration with national correspondents, WHO 

Regional Office for Europe and partners. The joint 

ECDC and World Health Organization Regional Office 

for Europe TB report, launched on 18 March, shows 

that tuberculosis is still a matter of concern in Europe. 

Tuberculosis Surveillance in Europe 2008 presents the 

latest data on TB cases and shows that the decline in 

cases has slowed down [11]. 

With the enhanced and improved regular surveillance 

of anti-TB drugs and molecular surveillance of MDR TB 

cases, ECDC is offering an added value to the European 

surveillance [9,10]. Surveillance is an integral part of 

TB control, its contribution being essential to inform 

the programme on what is going on and what public 

health response is urgently needed. Investing in better 

“intelligence” is a pre-requisite to improve TB prevention 

and control in Europe, in order to reach the elimination 

goal for Europe committed to in the early 1990s 

[8]. 

References 

1. Migliori GB, Sotgiu G, Lange C, Centis R. XDR-TB: back to the 

future. Eur Respir J. 2010; in press. 

2. Raviglione MC, Uplekar MW. WHO’s new Stop TB Strategy. 

Lancet. 2006;367(9514):952–5. 

3. Marica C, Didilescu C, Galie N, Chiotan D, Zellweger JP, Sotgiu 

G, et al. Reversing the tuberculosis upwards trend: a success 

story in Romania. Eur Respir J. 2009;33(1):168–70. 

4. Manissero D, Hollo V, Huitric E, Ködmön C, Amato-Gauci A. 

Analysis of tuberculosis treatment outcomes in the European 

Union and European Economic Area: efforts needed towards 

optimal case management and control. Euro Surveill. 

2010;15(11). pii=19514. Available online: http://www. 

eurosurveillance.org/ViewArticle.aspx?ArticleId=19514 

5. Devaux I, Manissero D, Fernandez de la Hoz K, Kremer K, van 

Soolingen D, on behalf of the EuroTB network. Surveillance of 

extensively drug-resistant tuberculosis in Europe, 2003-2007. 


Euro Surveill. 2010;15(11). pii=19518. Available online: http:// 

www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19518 

6. Ködmön C, Hollo V, Huitric E, Amato-Gauci A, Manissero D. 

Multidrug- and extensively drug-resistant tuberculosis: a 

persistent problem in the European Union European Union and 

European Economic Area. Euro Surveill. 2010;15(11). pii=19519. 

Available online: http://www.eurosurveillance.org/ViewArticle. 

aspx?ArticleId=19519 

7. Caley M, Fowler T, Welch S, Wood A. Risk of developing 

tuberculosis from a school contact: retrospective cohort study, 

United Kingdom, 2009. Euro Surveill. 2010;15(11). pii=19510. 

Available online: http://www.eurosurveillance.org/ViewArticle. 


8. Broekmans JF, Migliori GB, Rieder HL, Lees J, Ruutu P, 

Loddenkemper R, Raviglione MC; World Health Organization, 

International Union Against Tuberculosis and Lung 

Disease, and Royal Netherlands Tuberculosis Association 

Working Group. European framework for tuberculosis 

control and elimination in countries with a low incidence. 

Recommendations of the World Health Organization (WHO), 

International Union against Tuberculosis and Lung Disease 

(IUATLD) and Royal Netherlands Tuberculosis Association 

(KNCV) Working Group. Eur Respir J. 2002;19(4):765–75. 

9. Falzon D, Infuso A, Aït-Belghiti F. In the European Union, TB 

patients from former Soviet countries have a high risk of 

multidrug resistance. Int J Tuberc Lung Dis. 2006;10(9):954-8. 

10. Devaux I, Kremer K, Heersma H, Van Soolingen D. Clusters of 

multidrug-resistant Mycobacterium tuberculosis cases, Europe. 

Emerg Infect Dis. 2009;15(7):1052-60. This project applied 

to MDR TB only. The new dimension with ECDC is to apply 

molecular surveillance to all TB cases. 

11. European Centre for Disease Prevention and Control/WHO 

Regional Office for Europe: Tuberculosis surveillance in Europe 

2008. Stockholm, European Centre for Disease Prevention 

and Control, 2010. Available from: http://www.ecdc.europa. 

eu/en/publications/Publications/1003_SUR_tuberculosis_ 

surveillance_in_europe_2008.pdf 

3

Rapid communications 

Multidrug- and extensively drug-resistant tuberculosis: 

a persistent problem in the European Union and 

European Economic Area 

C Ködmön (csaba.kodmon@ecdc.europa.eu) 1 , V Hollo 1 , E Huitric 2 , A Amato-Gauci 3 , D Manissero 2 

1. Surveillance Unit, Tuberculosis Programme, European Centre for Disease Prevention and Control, Stockholm, Sweden 

2. Scientific Advice Unit, Tuberculosis Programme, European Centre for Disease Prevention and Control, Stockholm, Sweden 

3. Surveillance Unit, European Centre for Disease Prevention and Control, Stockholm, Sweden 


Ködmön C, Hollo V, Huitric E, Amato-Gauci A, Manissero D. Multidrug- and extensively drug-resistant tuberculosis: a persistent problem in the European 

Union European Union and European Economic Area. Euro Surveill. 2010;15(11):pii=19519. Available online: http://www.eurosurveillance.org/ViewArticle. 


Since 2008, the European Centre for Disease 

Prevention and Control has been collecting data from 

the European Union (EU) and European Economic Area 

(EEA) on resistance to first- and second-line drugs 

against tuberculosis (TB). In 2008, the proportion of 

multidrug-resistant tuberculosis (MDR TB) was 6.0% 

of the total case load for 25 countries reporting data. 

Extensively drug-resistant (XDR TB) reporting has 

increased since 2007 and was observed in 7.3% of 

the MDR TB cases in 13 reporting countries. MDR TB 

remains a threat and XDR TB is now established within 

the EU/EEA borders. 

Background 

Tuberculosis (TB) is among the leading causes of 

death due to a single pathogen worldwide. The World 

Health Organization (WHO) estimates that 32% of 

the world population is infected with Mycobacterium 

tuberculosis, the causative agent of tuberculosis [1], with 

9.2 million new TB cases and 1.7 million deaths from TB 

reported in 2007 [2]. Drug resistance to isoniazid and 

rifampicin (the definition for multidrug-resistant (MDR) 

TB), the two most potent first-line antimicrobial drugs 

for the treatment of TB, is a persisting global problem 

with surveillance data indicating increasing trends in 

several countries [3–7]. In 2007, the WHO reported the 

highest rates of MDR TB ever recorded, with up to 22% 

of new TB cases being resistant to both isoniazid and 

rifampicin in some areas of the former Soviet Union [2]. 

The increases in prevalence and incidence of MDR TB 

are caused by concurrent factors such as inadequate 

treatment regimens, poor case holding, suboptimal 

drug quality and transmission of resistant strains [8]. 

In recent years, public health awareness about MDR 

TB has been reinforced by the occurrence of extensively 

drug-resistant (XDR) TB outbreaks associated 

with human immunodeficiency virus (HIV) infections, 

particularly in South Africa [9,10]. XDR TB strains are 

defined as strains resistant to isoniazid and rifampicin 

(i.e. MDR) as well as to a fluoroquinolone and to one 


or more of the following injectable drugs: amikacin, 

capreomycin, or kanamycin). 

In Europe, the prevalence of MDR TB is high, particularly 

in some areas [4], and past surveillance reports 

have highlighted that MDR TB and XDR TB are a threat 

to TB control and elimination, also within the borders 

of the Member States of the European Union (EU) and 

European Economic Area (EEA) [11,12]. We therefore 

aimed at analysing the most recent data for the EU and 

EEA to describe the current MDR/XDR TB situation in 

this region. 

Methods 

Surveillance of drug resistance, based on annual casebased 

reporting of drug susceptibility testing (DST) 

results, has been ongoing in Europe since 1998 through 

the EURO-TB network and has included annual reporting 

of MDR TB cases [13]. Since 2008, the European 

Centre for Disease Prevention and Control (ECDC) and 

the WHO Regional Office for Europe have jointly been 

conducting TB surveillance for Europe. Data for the EU 

and EEA countries are reported to the ECDC through 

the European surveillance system, TESSy. 

Since the reporting year 1998, DST results from initial 

M. tuberculosis isolates have been collected for isoniazid, 

rifampicin, ethambutol and streptomycin. Since 

2009, DST data for MDR TB cases on fluoroquinolones 

(ciprofloxacin, ofloxacin) and second-line injectable 

anti-TB drugs (amikacin, kanamycin and capreomycin) 

have been collected and reports have included retrospective 

data from 2007 and 2008. In this study, data 

was extracted from TESSy for EU and EEA countries 

reporting resistance to first-line drugs for the reporting 

year 2008. For the reporting years 2007 and 2008, 

data was extracted for EU and EEA countries reporting 

resistance to second-line drugs for MDR TB cases. 


Table 1 

Combined (previously untreated and retreatment) anti-tuberculosis drug resistance in EU/EEA countries, 2008 

Cases resistant to at least: 

Cases resistant to 

any anti-TB drug 

Ethambutol Streptomycin 

Isoniazid and Rifampicin 

(multidrug-resistant) 

Isoniazid Rifampicin 

Cases with DST results 

to at least rifampicin and 

isoniazid1 Culture-positive 

cases 

Total number of 

cases 


Country N (%) N (%) N (%) N (%) N (%) N (%) N (%) N (%) 

Austria - - - - - - - - - - - - - - - - - 

Belgium 1,006 812 (80.7) 773 (95.2) 56 (7.2) 24 (3.1) 22 (2.8) 22 (2.8) 4 (0.5) 62 (8.0) 

Bulgaria 3,151 1,361 (43.2) 938 (68.9) 121 (12.9) 43 (4.6) 32 (3.4) 84 (9.0) 55 (5.9) 179 (19.1) 

Cyprus 50 36 (72.0) 36 (100.0) 4 (11.1) 1 (2.8) 1 (2.8) 0 (0.0) 3 (8.3) 6 (16.7) 

Czech Republic 868 561 (64.6) 520 (92.7) 26 (5.0) 14 (2.7) 11 (2.1) 7 (1.3) 29 (5.6) 41 (7.9) 

Denmark 367 283 (77.1) 281 (99.3) 11 (3.9) 0 (0.0) 0 (0.0) 1 (0.4) 0 (0.0) 12 (4.3) 

Estonia 444 347 (78.2) 347 (100.0) 103 (29.7) 74 (21.3) 74 (21.3) 78 (22.5) 122 (35.2) 130 (37.5) 

Finland 350 248 (70.9) 247 (99.6) 12 (4.9) 2 (0.8) 1 (0.4) 0 (0.0) 6 (2.4) 15 (6.1) 

France 5,812 2,296 (39.5) 1,556 (67.8) 103 (6.6) 32 (2.1) 27 (1.7) 18 (1.2) 112 (7.2) 171 (11.0) 

Germany 4,543 3,112 (68.5) 2,854 (91.7) 197 (6.9) 55 (1.9) 45 (1.6) 45 (1.6) 194 (6.8) 287 (10.1) 

Greece 669 - - - - - - - - - - - - - - - - 

Hungary 1,606 766 (47.7) 611 (79.8) 48 (7.9) 18 (2.9) 16 (2.6) 19 (3.1) 37 (6.1) 71 (11.6) 

Iceland 6 5 (83.3) 5 (100.0) 2 (40.0) 1 (20.0) 1 (20.0) 0 (0.0) 1 (20.0) 2 (40.0) 

Ireland 470 209 (44.5) 146 (69.9) 9 (6.2) 4 (2.7) 3 (2.1) 2 (1.4) 5 (3.4) 13 (8.9) 

Italy 4,418 2,026 (45.9) 1,932 (95.4) 244 (12.6) 89 (4.6) 71 (3.7) 71 (3.7) 238 (12.3) 381 (19.7) 

Latvia 1,070 838 (78.3) 828 (98.8) 257 (31.0) 132 (15.9) 129 (15.6) 115 (13.9) 242 (29.2) 285 (34.4) 

Liechtenstein - - - - - - - - - - - - - - - - - 

Lithuania 2,250 1,616 (71.8) 1,616 (100.0) 469 (29.0) 287 (17.8) 276 (17.1) 167 (10.3) 412 (25.5) 513 (31.7) 

Luxembourg 28 - - - - - - - - - - - - - - - - 

Malta 53 25 (47.2) 25 (100.0) 2 (8.0) 0 (0.0) 0 (0.0) 0 (0.0) 5 (20.0) 5 (20.0) 

Netherlands 997 728 (73.0) 728 (100.0) 55 (7.6) 14 (1.9) 13 (1.8) 3 (0.4) 0 (0.0) 56 (7.7) 

Norway 324 227 (70.1) 227 (100.0) 36 (15.9) 6 (2.6) 4 (1.8) 6 (2.6) 29 (12.8) 48 (21.1) 

Poland 8,081 5,094 (63.0) - - - - - - - - - - - - - - 

Portugal 2,995 2,007 (67.0) 1,641 (81.8) 121 (7.4) 29 (1.8) 28 (1.7) 17 (1.0) 156 (9.5) 213 (13.0) 

Romania 24,786 14,762 (59.6) 5,547 (37.6) 1,126 (20.3) 873 (15.7) 816 (14.7) 297 (5.4) 229 (4.1) 1,187 (21.4) 

Slovakia 633 383 (60.5) 383 (100.0) 10 (2.6) 4 (1.0) 4 (1.0) 2 (0.5) 3 (0.8) 12 (3.1) 

Slovenia 213 201 (94.4) 195 (97.0) 3 (1.5) 2 (1.0) 2 (1.0) 1 (0.5) 5 (2.6) 6 (3.1) 

Spain 8,214 4,493 (54.7) 1,628 (36.2) 161 (9.9) 88 (5.4) 76 (4.7) 32 (2.0) 77 (4.7) 191 (11.7) 

Sweden 552 436 (79.0) 423 (97.0) 49 (11.6) 13 (3.1) 12 (2.8) 15 (3.5) 9 (2.1) 52 (12.3) 

United Kingdom 8,655 4,870 (56.3) 4,808 (98.7) 288 (6.0) 71 (1.5) 53 (1.1) 35 (0.7) 186 (3.9) 405 (8.4) 

Total 82 611 47,7422 (57.8) 28,295 (66.3) 3,513 (12.4) 1,876 (6.6) 1,717 (6.1) 1,037 (3.7) 2,159 (7.6) 4,343 (15.3) 

DST: drug sensitivity testing; EEA: European Economic Area; EU: European Union; TB: tuberculosis. 

1 Any resistance to isoniazid, rifampicin, ethambutol or streptomycin, expressed as a percentage of cases with available DST results at least to isoniasid and rifampicin. Testing for ethambutol and 

streptomycin not routine in all countries. 

2 Total number of culture-positive cases excluding Poland, which did not report DST data: 42,648. 

5

The total number of cases, the total number of culturepositive 

cases and the total number of cases with DST 

results (sensitive or resistant to at least isoniazid and 

rifampicin) were extracted to assess the interpretability 

of DST data. 

The proportions of drug-resistant cases were calculated 

using the total number of cases with available 

DST results for at least isoniazid and rifampicin as a 

denominator; if these cases also included results for 

ethambutol and streptomycin, DST results for these 

antibiotics were also analysed. Cases of MDR TB 

were defined as cases resistant to at least isoniazid 

and rifampicin. In order to analyse findings on MDR 

Table 2 

Multidrug-resistant cases by previous history of tuberculosis treatment in the EU/EEA, 2008 

Country 

Cases with DST 

results 

TB among new and retreatment cases, MDR TB data 

among reported cases were stratified by history of previous 

treatment. New cases were defined as cases who 

had never previously received drug treatment for active 

TB, or who had received anti-TB drugs for less than one 

month. Retreatment cases were defined as cases who 

had received treatment with anti-TB drugs (excluding 

preventive therapy) for at least one month. 

Among MDR TB cases reported for 2007 and 2008, 

those with positive DST results for any of the reportable 

fluoroquinolones as well as to at least one of the 

reportable injectables were classified as XDR TB cases. 

The standard international definition for XDR TB was 

New Retreatment Treatment history unknown 

Multidrug-resistant Cases with DST 

results 

Multidrug-resistant Cases with DST 

results 

Multidrugresistant 

N (%) N (%) N (%) 

Austria - - - - - - - - - 

Belgium1 621 14 (2.3) 57 7 (12.3) 95 1 (1.1) 

Bulgaria 833 14 (1.7) 105 18 (17.1) 0 0 - 

Cyprus 11 0 (0.0) 3 1 (33.3) 22 0 (0.0) 

Czech Republic 483 10 (2.1) 37 1 (2.7) 0 0 - 

Denmark1 253 0 (0.0) 28 0 (0.0) 0 0 - 

Estonia 272 42 (15.4) 75 32 (42.7) 0 0 - 

Finland 238 1 (0.4) 9 0 (0.0) 0 0 - 

France 1,313 16 (1.2) 104 10 (9.6) 139 1 (0.7) 

Germany 2,450 16 (0.7) 153 21 (13.7) 343 8 (2.3) 

Greece - - - - - - - - - 

Hungary 509 8 (1.6) 97 6 (6.2) 5 2 (40.0) 

Iceland 4 1 (25.0) 0 0 (0.0) 1 0 (0.0) 

Ireland1 113 2 (1.8) 9 0 (0.0) 24 1 (4.2) 

Italy 1,018 27 (2.7) 165 24 (14.5) 749 20 (2.7) 

Latvia 684 83 (12.1) 144 46 (31.9) 0 0 - 

Liechtenstein - - - - - - - - - 

Lithuania 1,259 113 (9.0) 356 162 (45.5) 1 1 (100.0) 

Luxembourg - - - - - - - - - 

Malta 22 0 (0.0) 3 0 (0.0) 0 0 - 

Netherlands 696 11 (1.6) 23 2 (8.7) 9 0 (0.0) 

Norway1 174 1 (0.6) 20 2 (10.0) 33 1 (3.0) 

Poland - - - - - - - - - 

Portugal 1,496 19 (1.3) 145 9 (6.2) 0 0 - 

Romania 3,025 130 (4.3) 2,522 686 (27.2) 0 0 - 

Slovakia 300 1 (0.3) 61 2 (3.3) 22 1 (4.5) 

Slovenia 183 1 (0.5) 12 1 (8.3) 0 0 - 

Spain 1,080 31 (2.9) 174 23 (13.2) 374 22 (5.9) 

Sweden 341 7 (2.1) 38 4 (10.5) 44 1 (2.3) 

United Kingdom1 3,707 38 (1.0) 228 7 (3.1) 873 8 (0.9) 

Total EU/EEA 21,085 586 (2.8) 4,568 1,064 (23.3) 2,734 67 (2.5) 

DST: drug sensitivity testing; EEA: European Economic Area; EU: European Union; TB: tuberculosis. 

- : not reported 

1 Any resistance to isoniazid, rifampicin, ethambutol or streptomycin, expressed as a percentage of cases with available DST results at least 

to isoniasid and rifampicin. Testing for ethambutol and streptomycin not routine in all countries. 


therefore applied [14]. Changes in the prevalence of 

XDR TB among MDR TB cases between 2007 and 2008 

were analysed. 

Findings 

In 2008, 47,742 culture-positive TB cases were 

reported by 27 EU and EEA Member States. This represents 

57.8% of the total TB case load (82,611), with 

the percentage ranging from 36.2% to 100% among 

the reporting countries (Table 1). Data on resistance to 

first-line drugs in 2008 were available for 25 countries, 

representing a total of 28,295 cases (66.3% of the total 

culture-positive cases, excluding culture-confirmed 

cases from Poland as DST data was not reported) 

(Table 1). 

In 2008, the proportion of culture-positive TB cases 

resistant to any first-line anti-TB drug was 15.3% 

(N=4,343). The proportion of resistance to either isoniazid 

or rifampicin among culture-positive cases was 

12.4% (N=3,513) and 6.6% (N=1,876), respectively 

(Table 1). The proportion of combined (new and retreatment) 

MDR TB cases in the 25 countries was 6.0%, as 

shown in Table 1. The Baltic States (Latvia, Lithuania 

and Estonia) and Romania showed the highest proportions 

(15.6%, 17.1% 21.3% and 14.7%, respectively) 

of MDR TB cases (Table 1). The overall proportion of 

MDR TB among new cases was 2.8%, ranging from 

0% to 25%, and was again highest in the Baltic States 

(9.0%–15.4%) and Iceland (25.0%, one case). Among 

retreatment cases, the overall proportion of MDR cases 

was 23.2%, with the highest proportions in the Baltic 

States (31.9%-45.5%), Cyprus (33.3%, one case) and 

Romania (27.2%) (Table 2). 

Thirteen countries provided data on resistance to second-line 

drugs, allowing the identification of XDR TB 

Table 3 

Extensively drug-resistant tuberculosis cases in the EU/EEA, 2007-2008 


Total MDR-TB Total XDR-TB 

XDR/MDR 

% 

cases for the reporting years 2007 and 2008. Among 

the total of 1,122 MDR TB cases (new and retreatment 

cases) reported by these 13 countries in 2007, 

68 were XDR TB cases, representing 6.1% of the total 

MDR TB burden. In 2008, 90 XDR TB cases were notified, 

with the proportion of XDR TB cases among MDR 

TB cases increasing to 7.3%. Latvia and Romania had 

the highest number of XDR TB cases in 2008 (19 and 54 

cases, respectively). In Estonia, a decline in the total 

number and proportion of XDR TB cases from 12 to 

nine cases (15.0% to 12.2%) was observed compared 

to 2007, while in Latvia had an increase in the number 

of reported XDR TB cases in 2008 relative to 2007 from 

six to 19 cases (6.1% to 14.7%) (Table 3). 

Conclusions 

The data highlight two important findings concerning 

the MDR/XDR TB situation in the EU/EEA Member 

States. First, it is evident that reporting completeness 

remains suboptimal in this region. In particular, the 

percentage of the total TB case load for which the drug 

resistance profile for at least isoniazid and rifampicin is 

known, remains low. The DST results were available for 

only 34.4% of the total notified cases (28,295 of 82,611 

cases in 2008), reflecting a low culture positivity rate 

(57.5%) and a low DST coverage (66.4% of culturepositive 

cases). This represents not only a surveillance 

limitation, but it could also hamper the implementation 

of proper TB control practices such as infection control 

and case management. 

Secondly, the data highlights the fact that MDR TB 

persists as a threat to the EU/EEA. This is underlined 

by four of the five WHO High Priority Countries within 

the EU/EEA (Estonia, Latvia, Lithuania and Romania) 

reporting proportions of combined MDR TB of well over 

10% of the total case load [15]. The analysis of MDR 

Total MDR-TB Total XDR-TB 

XDR/MDR 

% 

Belgium 14 1 (7.1) 22 2 (9.1) 

Bulgaria 76 0 (0.0) 32 0 (0.0) 

Cyprus 3 0 (0.0) 1 0 (0.0) 

Czech Republic 8 0 (0.0) 11 1 (9.1) 

Estonia 80 12 (15.0) 74 9 (12.2) 

Iceland 1 0 (0.0) 1 0 (0.0) 

Latvia 99 6 (6.1) 129 19 (14.7) 

Norway 3 1 (33.3) 4 0 (0.0) 

Romania 701 47 (6.7) 816 54 (6.6) 

Slovakia 7 0 (0.0) 4 0 (0.0) 

Spain 59 0 - 76 3 (3.9) 

Sweden 15 1 (6.7) 12 1 (8.3) 

United Kingdom 56 0 (0.0) 53 1 (1.9) 

Total EU/EEA 1,122 68 (6.1) 1,235 90 (7.3) 

MDR: multidrug-resistant; EEA: European Economic Area; EU: European Union; TB: tuberculosis; XDR: extensively drug-resistant. 

7

TB reporting can be used to indicate weaknesses in 

TB control programmes. The high proportion of MDR 

TB among new TB cases reported by certain countries 

could suggest suboptimal infection control, whilst the 

high percentage of MDR TB among retreatment cases 

(23.3%) could suggest poor case holding and followup 

or suboptimal use of TB regimens during the past 

decade. 

For the first time since the surveillance of anti-TB 

drugs has been performed at EU level, notification 

data on XDR TB is available through the joint surveillance 

system. Although the quality and completeness 

of second-line resistance data remains questionable, 

the numbers confirm that XDR TB is now established in 

the EU. The increase of 32.4% in reported XDR TB cases 

is difficult to interpret as this could well represent an 

improvement in DST coverage for second-line drugs, as 

opposed to representing a true increase in the prevalence 

of XDR TB. 

The link and interdependence between TB surveillance, 

TB case management and control of drug-resistant TB 

is well reflected by these data. Improvement in the 

quality and completeness of MDR/XDR TB surveillance 

data is needed. This will be achieved by the countries’ 

serious commitment to optimise TB control practices 

as well as improve TB case management, which in turn 

should reverse the of MDR/XDR TB trends observed in 

recent years. 

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ML, Drobniewski F, Hoffner SE, Raviglione MC, et al. 

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http://www.euro.who.int/document/E91049.pdf 



Surveillance of extensively drug-resistant tuberculosis in 

Europe, 2003-2007 

I Devaux (Isabelle.Devaux@ecdc.europa.eu) 1,2 , D Manissero 3 , K Fernandez de la Hoz 3,4 , K Kremer 5 , D van Soolingen 5 , on behalf of 

the EuroTB network 6 

1. EuroTB, Institut National de Veille Sanitaire (InVS), Saint Maurice, France (affiliation where the work was performed) 

2. Current affiliation: European Centre for Disease Prevention and Control (ECDC), Stockholm, Sweden 

3. European Centre for Disease Prevention and Control, Stockholm (ECDC), Sweden 

4. Current affiliation: Dirección General de Salud Pública y Sanidad Exterior, Madrid, Spain 

5. National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands 

6. The members of the network are listed at the end of the article 


Devaux I, Manissero D, Fernandez de la Hoz K, Kremer K, van Soolingen D, on behalf of the EuroTB network. Surveillance of extensively drug-resistant tuberculosis 

in Europe, 2003-2007. Euro Surveill. 2010;15(11):pii=19518. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19518 

This paper describes the results of second-line drug 

(SLD) susceptibility tests among multidrug-resistant 

tuberculosis (MDR TB) cases reported in 20 European 

countries aiming to identify extensively drug-resistant 

tuberculosis (XDR TB) cases. A project on molecular 

surveillance of MDR TB cases was conducted by 

EuroTB and the National Institute for Public Health 

and the Environment (RIVM) from 2005 to 2007. 

Information on drug susceptibility testing (DST) was 

provided to this project and case-based data on MDR 

TB cases were reported on a quarterly basis by 20 

countries of the World Health Organization’s European 

Region, including 15 European Union Member States. 

Data included SLD susceptibility test results, enabling 

a retrospective description of XDR TB cases notified 

between 2003 and 2007. In 18 countries DST was 

performed for two or more of the SLD included in the 

XDR TB definition. The proportion of MDR TB isolates 

tested for SLD varied widely between countries (range 

20 to 100 percent). In the 18 countries, 149 (10%) XDR 

TB cases were reported among MDR TB cases with 

available DST results for SLD. Sixteen additional MDR 

TB cases were reported by the MDR TB surveillance 

system when compared with the number of routinely 

reported MDR TB cases to EuroTB in ten countries with 

representative data reported during three consecutive 

years (2003-2005). To counter the threat of XDR TB in 

Europe, a standardised approach to XDR TB surveillance 

and DST for SLD is needed, as well as increased 

laboratory capacity across European countries. 

Introduction 

Extensively drug-resistant tuberculosis (XDR TB) is 

a worldwide threat to TB control, as XDR TB cases 

are extremely difficult to treat [1]. The origin of XDR 

TB is linked to the introduction of second-line antituberculosis 

drugs (SLD) for the treatment of multidrug-resistant 

tuberculosis (MDR TB) and the possible 

mismanagement of patients (including failure of compliance) 

under SLD treatment [2,3]. In March 2006, the 



term XDR TB first appeared in the literature in a United 

States Centers for Disease Control and Prevention (US 

CDC) report describing the findings of a worldwide 

survey on anti-TB drug resistance carried out between 

2000 and 2004 [4]. Since then, a number of scientific 

and media reports on XDR TB have been published 

[5]. Although the term has emerged only recently, the 

occurrence of TB cases resistant to most available 

drugs is not new [6]. The definition of XDR TB, MDR TB 

plus resistance to a fluoroquinolone and at least one of 

three injectable SLD (amycacin, kanamycin, capreomycin) 

has been revised in 2006 because not all the SLD 

included in the original case definition were used and 

tested worldwide [7-9]. 

Epidemics of drug-resistant TB have been described in 

the WHO European Region since the 1990s [10]. XDR TB 

has been identified as a significant problem in countries 

of the former Soviet Union [11] and the potential 

threat of XDR TB for Europe has been assessed by the 

European Centre for Disease Centre and Prevention 

(ECDC) in 2006 [12]. The occurrence of XDR TB outbreaks 

in patients co-infected with HIV has re-enforced 

the public health awareness, with a particular focus on 

South Africa [13]. 

In 2005, the EuroTB network started a molecular 

surveillance project on MDR TB in 24 countries of 

the WHO European Region including 19 European 

Union (EU) Member States, plus Croatia, Israel, the 

Former Yugoslav Republic of Macedonia, Norway and 

Switzerland) [14]. The project was coordinated by 

EuroTB in France and the National Institute for Public 

Health and the Environment (RIVM) in the Netherlands 

until the end of 2007. As resistance to SLD was already 

a matter of concern in 2005, data on drug susceptibility 

testing (DST) for SLD were collected in addition to 

DNA fingerprint data [14,15]. The project provided an 

opportunity to implement case reporting of XDR TB by 

applying the revised XDR TB case definition of 2006 

9

etrospectively. This article describes notification data 

on resistance to SLD in the EU and some neighbouring 

countries from January 2003 through June 2007. 

Methods 

Data collection 

The MDR TB project included 24 countries of the WHO 

European Region that were able to or planning to participate 

in case-based reporting of molecular data on 

MDR TB cases at European level in 2005. Case-based 

data on all newly diagnosed and culture confirmed 

positive MDR TB cases were reported by national 

surveillance institutions (NSI) to EuroTB on a quarterly 

basis from January 2005 through June 2007. Data for 

2003 and 2004 were reported retrospectively. The data 

were collected anonymously, according to a standardised 

data file specification reviewed by the members 

of the EuroTB advisory committee [16]. Each case had 

a unique record identifier. Common definitions of variables 

were used by the participating countries, including 

demographic and clinical variables and results from 

susceptibility testing for first and second-line anti-TB 

drugs. The country of origin of a case was defined as 

Table 1 

Reporting of anti-tuberculosis second line DST on Mycobacterium tuberculosis isolates of MDR TB cases in 20 European 

countries, 2003-2007 1 

MDR TB Secondline 

Injectable drugs Fluoroquinolones 

Country 

cases drugs tested Amikacin Kanamycin Capreomycin Ciprofloxacin Ofloxacin 

N 

N 

N (%) N (%) N (%) N (%) N (%) 

Five second line anti-tuberculosis drugs tested 

France2 152 5 148 (97) 147 (97) 135 (89) 145 (95) 149 (98) 

Czech Republic1 38 5 25 (66) 22 (58) 25 (66) 25 (66) 25 (66) 

Norway1 11 5 11 (100) 11 (100) 11 (100) 5 (45) 11 (100) 

Ireland1 8 5 3 (38) 1 (13) 3 (38) 3 (38) 1 (13) 

Slovenia4 3 5 3 (100) 1 (33) 1 (33) 3 (100) 1 (33) 

Four second line anti-tuberculosis drugs tested 

Lithuania3 656 4 89 (14) 173 (26) 101 (15) - - 172 (26) 

Estonia2 248 4 245 (99) 245 (99) 244 (98) - - 245 (99) 

Israel2 45 4 43 (96) - - 43 (96) 44 (98) 44 (98) 

Switzerland1 25 4 24 (96) - - 9 (36) 4 (16) 19 (76) 

Denmark3 5 4 5 (100) - - 5 (100) 5 (100) 5 (10) 

Three second line anti-tuberculosis drugs tested 

Latvia1 712 3 - - 705 (99) 698 (98) - - 689 (97) 

Romania3 50 3 19 (38) 44 (88) - - 44 (88) - - 

Belgium1 31 3 12 (39) 2 (6) - - - - 12 (39) 

Poland4 17 3 6 (35) - - 6 (35) - - 6 (35) 

Former Yugoslavian Republic 

of Macedonia1 15 3 8 (53) - - 8 (53) 8 (53) - - 

Cyprus1 3 3 1 (33) - - 3 (100) - - 3 (10) 

Two second line anti-tuberculosis drugs tested 

The Netherlands2 34 2 33 (97) - - - - 34 (100) - - 

Croatia2 5 2 1 (20) - - - - 2 (40) - - 

One second line anti-tuberculosis drug tested 

Spain3 50 1 - - 2 (4) - - - - - - 

Sweden1 21 1 15 (71) - - - - - - - - 

Total 2,129 691 (51) 1,353 (69) 1,292 (67) 322 (82) 1382 (71) 

DST: drug sensitivity testing; MDR TB: multidrug-resistant tuberculosis. 

1 Data reported between 2003 and 2007. 



4 Data reported in 2005 and 2006 in Poland ; 2003 and 2005 in Cyprus; 2003, 2005 and 2006 in Slovenia. 


their country of birth (if available) or their country of 

citizenship. 

Reporting of drug susceptibility testing for 

second-line drugs and XDR TB cases 

DST results for SLD, resistant or susceptible, were collected 

for the following drugs: amikacin, kanamycin, 

capreomycin, ciprofloxacin, ofloxacin. The rationale 

behind the choice of the SLD tested was that they represented 

the most commonly used aminoglycosides 

(injectables) and fluoroquinolones. If no resistance is 

measured against the tested drugs within each of these 

two classes of drugs, it is unlikely that resistance can 

be found against other drugs from the same classes, 

because of cross-resistance. Data were validated by 

EuroTB, eventually completed by the reporting NSI and 

collated into a European MDR TB case database. 

The revised 2006 XDR TB case definition was used 

for the analysis [8]. This definition refers to XDR TB 

as resistance to at least isoniazid and rifampicin 

as well as further resistance to a fluoroquinolone 

(ofloxacin, ciprofloxacin) and at least one second-line 

injectable aminoglycocide (amikacin, kanamycin and 

capreomycin). 


The number and distribution of MDR TB isolates tested 

for anti-TB second-line DST as well as the number and 

proportion of XDR TB cases by country were calculated. 

The percentage of SLD tested (SLD testing percentage) 

for a given country was defined as the number of tests 

performed for a specific drug divided by the number of 

MDR TB cases reported in that country. The proportion 

of XDR TB cases was calculated using the number of 

MDR TB cases tested for SLD (included in the XDR TB 

definition) as a denominator. 

As reported by EuroTB [17], anti-TB drug resistance surveillance 

(DRS) was performed on nationwide samples 

of TB cases in all 18 countries participating to the MDR 

TB project [14], except for Italy and Spain (partial coverage) 

and Poland (no information about representativeness 

available). Data from Romania was provided 

from a country-wide DST survey. 

The number of MDR TB cases reported to the 

project was compared with the number of MDR TB 

cases reported to Euro-TB using drug resistance 

susceptibility data. 

Table 2 

Distribution of MDR and XDR TB cases by country reported in 18 European countries, 2003-2007 1 

MDR TB cases reported to MDR TB isolates tested for 

XDR among MDR TB cases 

Country (number of TB cases 

XDR TB cases 

MDR TB project 

2-5 SLD 

with SLD DST 

reported to EuroTB) 

N 

N 

Countries with at least 88% of MDR TB cases tested for two to five SLD 

N (%) 

% 

Latvia (6,107) 712 688 (97) 53 8 

Estonia (1,736) 248 245 (99) 58 24 

France (16,986) 152 149 (98) 1 1 

Romania (60,323) 50 44 (88) 2 5 

Israel (1,454) 45 44 (98) 2 5 

Netherlands (3,820) 34 33 (97) 1 3 

Switzerland (2,303) 25 22 (88) 0 0 

Norway (1,221) 11 11 (100) 0 0 

Denmark (1,200) 5 5 (100) 0 0 

Slovenia (1,049) 3 3 (100) 1 33 

Cyprus (102) 3 3 (100) 0 0 

Total 1,288 1,247 (97) 118 9% 

Countries with less than 88% of MDR TB cases tested for two to five SLD 

Lithuania (5,088) 656 173 (26) 25 14 

Czech Republic (4199) 38 25 (66) 5 20 

Belgium (4,187) 31 12 (39) 0 0 

Poland (17,873) 17 6 (35) 0 0 

Macedonia (2,662) 15 8 (53) 0 0 

Ireland (1,747) 8 3 (38) 1 33 

Croatia (3,931) 5 1 (20) 0 0 

Total 770 228 (30) 31 14% 

Total 2,058 1,475 (72) 149 10% 

DST: drug sensitivity testing; MDR TB: multidrug-resistant tuberculosis, XDR TB: extensively drug-resistant tuberculosis; SLD: second line 

drugs. 

1 Data reported for at least one year between 2003 and 2007. 

11

Results 

Individual data on SLD testing for Mycobacterium 

tuberculosis isolates from 2,129 cases reported 

between January 2003 and July 2007 were available 

for 20 countries (population of 259,467,657) out of 

24 European countries (population of 467,007,506), 

including 15 EU countries. Data were not reported by 

Germany, Italy, Finland and the United Kingdom, representing 

almost half of the total population covered by 

the surveillance project. 

Sixteen additional MDR TB cases were reported by the 

MDR TB surveillance system when compared with the 

number of routinely reported MDR TB cases to EuroTB 

in ten countries with representative data reported during 

three consecutive years (2003-2005) (i.e. Belgium, 

Denmark, Estonia, Ireland, Israel, Latvia, Netherlands, 

Norway, Slovenia, Switzerland) [17]. 

Number of second-line anti-TB drugs 

tested for susceptibility by country 

The number of SLD tested varied from one to five by 

country (Table 1). 

In the five countries where SLD testing was reported for 

all five drugs; France, Czech Republic, Norway, Ireland, 

and Slovenia, the proportion of MDR TB cases tested 

(SLD testing percentages) varied from ≥ 13% in Ireland 

to ≥ 58% in the Czech Republic, and ≥ 89% in France. In 

countries where DST was performed for four SLD, ciprofloxacin 

was not tested in Lithuania and Estonia, and 

kanamycin was not tested in Israel, Switzerland, and 

Denmark. Testing percentages were very high (≥ 96%) 

in Estonia and Israel for all the SLD tested. In contrast, 

testing percentages were low in Lithuania (≤ 26%). 

In the six countries where DST was performed for three 

drugs, amikacin was included in testing practices in 

all the countries, except in Latvia. DST was performed 

for two drugs (amikacin and ciprofloxacin) in the 

Netherlands (testing percentage ≥ 97%) and Croatia 

(testing percentage ≤ 40%). Two countries, Sweden and 

Spain tested for one SDL. 

In six countries (Norway, Ireland, Slovenia, Denmark, 

Cyprus and Croatia), the numbers of MDR TB cases 

reported was small and therefore the results for those 

countries do not necessarily reflect the testing practices 

in these countries. 

XDR TB cases reported by country 

The number of XDR TB cases was calculated for the 

18 countries where MDR TB isolates were tested for 

at least two SLD (Table 2). When considering the proportion 

of MDR TB cases tested for SLD, two groups of 

countries could be distinguished: group 1, countries 

with a high (≥ 88%) percentage of SLD testing and 

group 2, countries with a low (≤ 88%) percentage of 

SLD testing (Table 2). The ten countries in group 1 represented 

63% (1,288/2,058) of reported MDR TB cases 

and 79% of the identified XDR TB cases. 

XDR TB cases were detected in 10 countries, of which 

nine are EU Member States, and seven belonged to 

group 1. The overall proportion of XDR TB cases among 

MDR TB cases with DST for SLD was 10%. Ninety-one 

percent (136/149) of the XDR TB cases detected were 

reported in the Baltic States, where the percentage of 

XDR TB among MDR TB patients tested for SLD was 8% 

or higher (Table 2). In Estonia, 24% of MDR TB cases 

with DST results for SLD were XDR. This percentage 

is based on a highly representative sample of 99% of 

MDR TB patients tested for SLD. Therefore, this result 

indicates a relatively high prevalence of XDR TB among 

MDR TB cases in this country. In Latvia, where SLD 

results were available for 97% of MDR TB, the proportion 

of XDR TB was three times lower than in Estonia. 

In Lithuania, the proportion of XDR TB (14%) was based 

on a sample of 173 MDR TB cases with DST results. 

These 173 patients represent 26% of all reported MDR 

TB cases, which may not have been selected randomly 

meaning that only the most severe cases may have 

been tested for SLD. In the Czech Republic, the percentage 

of XDR TB cases was relatively high (20%), but 

the information for SLD testing was only available for 

25 cases, representing 66% of the Czech MDR TB cases 

reported to our project. 

Discussion 

This surveillance-based project provides baseline 

data on XDR TB in a large number of European countries 

at the time of the establishment of the XDR TB 

case definition. Although four western European countries 

with a large population were not included in this 

project, results show that at least one XDR TB case 

was reported in 10 out of 18 European countries. The 

overall proportion of XDR TB among 1,475 (72%) MDR 

TB patients tested for SLD was approximately 10%. 

Ninety-one percent of the reported 149 XDR TB cases 

were notified by the three Baltic countries (Estonia: 

248 cases, Latvia: 712 cases, Lithuania: 656 cases), 

which belonged to the former Soviet Union until 2004. 

This confirms the finding of a worldwide survey conducted 

by WHO and the US CDC, showing that the proportion 

of XDR TB among TB patients originating from 

former Soviet Union countries is high [18]. 

These data have to be interpreted in a broader scope of 

the establishment of TB surveillance and control in the 

WHO European Region [19,20]. The number of XDR TB 

cases detected can partly be affected by differences in 

surveillance systems between countries for case definitions, 

the possibility of linking laboratory and notification 

data, and by data quality (completeness and 

validity). The revision of the XDR TB definition had an 

impact on the determination of the number of XDR TB 

cases in European countries [8]. According to the previous 

case definition, the proportion of XDR among MDR 

TB cases was estimated to be higher in 17 countries 

[12]. 

The fact that 20 out of 24 participating countries 

reported SLD test results for at least one drug, and that 


DST for SLD was performed but not available for reporting 

in at least one other country, the United Kingdom, is 

a positive indicator for the availability of DST for SLD at 

European level. However, the number of XDR TB cases 

reported could be underestimated because of the limited 

number of SLD susceptibility testing in some countries 

or over-estimated due to lack of standardisation. 

The number and type of SLD tested varied considerably 

between countries. A lack of standardisation and homogeneity 

in drug susceptibility testing practices for SLD 

has been identified by a panel of laboratory experts 

[21]. However, susceptibility testing of SLD has yielded 

reliable and reproducible results for some of the SLD 

[22]. Cross-resistance is common among aminoglycosides 

and absolute among fluoroquinolones, however, 

not all isolates exhibit the same resistance profile. 

Despite issues related to cross-resistance, it remains 

important to test a broad panel of SLD [23]. At the time 

of reporting, SLD DST methods had not been standardised 

or recommended, and External Quality Assurance 

(EQA) was not available, but since 2007 EQA for SLD 

has begun and since 2008 policy guidance has been 

published, which should help in standardising testing 

practices [21]. Therefore, it is expected that SLD DST 

practices and standardisation of these will improve 

significantly within the coming years. 

The findings of this project and previous ones [14,18] 

concerning the relatively high rate of 10% XDR among 

MDR TB cases, should have an impact on clinical management 

of individual patients and TB control, especially 

in eastern European countries. There is a need 

for new drugs and treatment strategies. However, 

while new drugs will only be available in a number of 

years, the utility of derivates of current drugs and also 

alternative drugs like meropenem should be explored 

[24]. Serious consequences for TB control may be 

related to increased travel and migration, as this can 

lead to imported cases MDR TB from eastern Europe to 

western Europe, and transmissible forms of MDR and 

XDR TB are a fearsome scenario [14]. If transmission of 

XDR TB is diagnosed in western European countries, 

new strategies on monitoring risks associated with 

immigration from and travel to high-incidence settings 

should be developed. 

Our surveillance project has some limitations that 

should be taken into account in future MDR and XDR 

TB surveillance in Europe. It would be of considerable 

value if data from the four missing countries could be 

added. In countries with a low proportion of patients 

tested for SLD, (Lithuania, Czech Republic), additional 

data is needed to better interpret the XDR TB prevalence. 

In countries with low numbers of XDR TB cases 

reported (e.g. Ireland and Slovenia), XDR TB percentages 

can be biased and therefore should not be compared 

to other countries. 


Conclusion 

Further research are conducted on the occurrence of 

transmitted MDR and XDR TB strains to investigate 

whether they pose a new evolutionary development of 

M. tuberculosis, or an extend of the current problem. 

Both scenarios would highlight consequences of a long 

lasting, uncontrolled problem and demonstrate the 

need for enhanced efforts in TB control in the regions 

where this problem develops. The capacity for SLD testing 

should be upgraded, especially in areas with high 

numbers of drug-resistant TB cases, such as in eastern 

Europe. As identified in a previous survey [25], standardisation 

and quality assurance of laboratory methods 

for DST of SLD should be improved across Europe. 

An EU reference laboratory network has been established 

with EU Member States to support their activities 

[26]. Surveillance data on MDR and XDR TB with 

improved quality are essential to determine the magnitude 

of this threat to TB control. In addition, surveillance 

data is needed to monitor TB control activities, 

and as a basis for implementing appropriate treatment 

and care and to prioritise laboratory resources. 

The members of the EuroTB network were: M Wanlin, Belgium; G 

Vankerschaever, Belgium; M Fauville-Dufaux, Belgium; F Portaels, 

Belgium; A Simunovic, Croatia; V Katalinic-Jankovic, Croatia; D 

Pieridou-Bagatzouni, Cyprus; M Havelkova, Czech Republic; V 

Ostergaard Thomsen, Denmark; Z Kamper Jorgensen, Denmark; V 

Hollo, Estonia; T Kummik, Estonia; P Ruutu, Finland; M Marjamaki, 

Finland; J Makinen, Finland; D Che, France; D Antoine, France; C 

Gutierrez, France; J Robert, France; W Haas, Germany; B Brodhun, 

Germany; S Rüsch-Gerdes, Germany; S Niemann, Germany; J 

O’Donnell, Ireland; T Rogers, Ireland; M G Pompa, Italy; D Cirillo, 

Italy; A Gori, Italy; D Chemtob, Israel; D Goldblatt, Israel; V 

Riekstina, Latvia; G Skenders, Latvia; A Sosnovskaja, Lithuania; 

P Stakenas, Lithuania; A Vidoevska, Macedonia; H Heersma, 

The Netherlands; C Erkens, The Netherlands; B Askeland Winje, 

Norway; U R Dale, Norway; Z Zwolska, Poland; E Ibraim, Romania; 

D I Chiotan, Romania; I Solovic, Slovakia; J Trenkler, Slovakia; D 

Erzen, Slovenia; M Zolnir-Dovc, Slovenia; E Rodriguez Valin, Spain; 

S Samper, Spain; J Iglesias, Spain; V Romanus, Sweden; S Hoffner, 

Sweden; G Källenius, Sweden; P Helbling, Switzerland; B Springer, 

Switzerland; E C Boettger, Switzerland; J Watson, United Kingdom; 

I Abubakar, United Kingdom, Francis Drobniewski, United Kingdom. 

Acknowledgements 

We would like to thank the following contributors to this paper: 

Dennis Falzon, Andrea Infuso, Jean-Claude Desenclos, 

Delphine Antoine and Didier Che from the Institut National 

de Veille Sanitaire, in Paris, France as well as the members 

of the EuroTB Advisory Committee: Luke Clancy, Michael 

Forssbohm, Jean-Paul Klein, Maria Korzeniewska-Kosela, 

Vincent Kuyvenhoven and Richard Zaleskis. We also would 

like to thank Andrea Ammon, Abigail Wright, Mateo Zignol. 

The sources of financial support are the European 

Commission, DG-SANCO under the grant agreement no 

2004213 and the Institut National de Veille Sanitaire, France. 

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Analysis of tuberculosis treatment outcomes in the 

European Union and European Economic Area: efforts 

needed towards optimal case management and control 

D Manissero (davide.manissero@ecdc.europa.eu) 1 , V Hollo 2 , E Huitric 1 , C Ködmön 2 , A Amato-Gauci 3 

1. Scientific Advice Unit, Tuberculosis Programme, European Centre for Disease Prevention and Control, Stockholm, Sweden 

2. Surveillance Unit, Tuberculosis Programme, European Centre for Disease Prevention and Control, Stockholm, Sweden 

3. Surveillance Unit, European Centre for Disease Prevention and Control, Stockholm, Sweden 


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needed towards optimal case management and control. Euro Surveill. 2010;15(11):pii=19514. Available online: http://www.eurosurveillance.org/ViewArticle. 


An analysis of surveillance data was performed to 

assess treatment outcomes of patients belonging to 

selected calendar year cohorts. Twenty-two countries 

in the European Union (EU) and European Economic 

Area (EEA) reported treatment outcome monitoring 

data for culture-confirmed pulmonary tuberculosis 

(TB) cases reported in 2007. The overall treatment 

success rate was 73.8% for all culture-confirmed pulmonary 

cases and 79.5% for new culture-confirmed 

pulmonary cases. For the cohort of new culture-confirmed 

TB cases, only three countries achieved the 

target of 85% success rate. This underachievement 

appears to be a result of relative high defaulting and 

unknown outcome information. Case fatality remains 

high particularly among cases of national origin. This 

factor appears attributable to advanced age of the 

national cohort. Treatment outcomes for multidrugresistant 

tuberculosis were reported by 15 countries, 

with a range of 19.8% to 100% treatment success at 

24 months. The data underline the urgent need for 

strengthening treatment outcome monitoring in the 

EU and EEA in order to ensure an effective programme 

implementation and case management that will ultimately 

contribute to TB elimination. 

Background 

Tuberculosis (TB) remains a global emergency with 

estimates of 1.8 millions deaths worldwide in 2008 and 

over nine million cases. In 2008, the estimated global 

incidence rate fell to 139 cases per 100,000 population 

after reaching its peak in 2004 at 143 per 100,000. 

However, this decline was not homogeneous throughout 

the World Health Organization (WHO) regions, with 

Europe failing to record a substantial decline, but rather 

appearing to have reached a stabilisation of rates [1]. 

The 30 Member States of the European Union (EU) and 

European Economic Area (EEA) present a peculiar and 

highly heterogeneous situation in terms of TB epidemiology 

and control. Three broad epidemiological areas 

are distinguished within the borders of the EU/EEA: 

low incidence countries (below 20 notified cases per 



100,000 population) with cases aggregating in vulnerable 

populations and only occasional increased notification 

rates; countries with moderate-to-high, but 

declining notification rates and with a low proportion 

of multidrug-resistant (MDR) TB; and finally, countries 

with relatively high notification rates (over 100 notified 

cases per 100,000) and high levels of MDR TB, but 

again with declining overall TB rates [2-4]. 

Attention to TB control in the EU and EEA has been 

raised in recent years through a number of initiatives, 

including the launching of a Framework Action Plan to 

Fight Tuberculosis in the EU [5]. Among the key issues 

underlined in the Action Plan is the need to achieve and 

sustain acceptable levels of treatment success among 

all TB patients. 

Treatment success measured by a standardised process 

of treatment outcome monitoring (TOM) is one of 

the pillars of TB control and, along with case detection, 

is recognised as a key programmatic output. It 

is against this rationale that a World Health Assembly 

(WHA) resolution was passed in 1991, adopting two 

targets for global TB control: to detect at least 70% of 

new infectious cases and to cure at least 85% of those 

detected. These targets were linked to the Millennium 

Development Goals, and the Stop TB Partnership set 

the year 2005 as the deadline for achievement [6-8]. 

Globally, the treatment success rate has exceeded the 

85% target for the first time in 2008 since the target 

was set in 1991, with a percentage of 87% for patients 

starting treatment in 2007. Furthermore, treatment 

success rates were maintained or improved between 

2006 and 2007 in all WHO regions with the exception 

of the European Region which recorded the lowest success 

rate globally at 67% [1]. 

The importance of strengthening treatment outcome 

monitoring in Europe has long been recognised. 

A statement put forward by the WHO and the 

International Union against Tuberculosis and Lung 

15

Disease underlined in 1998 the need for standardisation 

and evaluation of treatment results for TB patients 

in the WHO European region, including those in low 

and intermediate incidence countries [9]. 

In this study we aimed to analyse treatment outcomes 

and progress towards the targets specifically for 

the EU/EEA region as a whole and its Member States 

separately. 

Since 1 January 2008, the European Centre for Disease 

Prevention and Control (ECDC) and the WHO Regional 

Office for Europe have jointly coordinated the TB surveillance 

in Europe. Designated national surveillance 

institutions or individuals are responsible for providing 

the data, which is reported to a central joint database. 

Furthermore, historical data are available from 

the former EuroTB project for TB surveillance activities 

in Europe from 1996 to 2007. These data represent a 

valuable source for an in-depth analysis of treatment 

outcome monitoring and were used in our study. 

Methods 

A descriptive analysis of surveillance data was performed 

to assess treatment outcomes of patients 

belonging to selected calendar year treatment cohorts. 

Figure 1 

Treatment outcome of laboratory-confirmed pulmonary cases, EU/EEA countries 1 2003-2007 

Proportion of cases (%) 

100 

90 

80 

70 

60 

50 

40 

30 

20 

10 

0 

Data were extracted from The European Surveillance 

System (TESSy) and from the former EuroTB historical 

database for the 30 EU and EEA countries reporting 

data to the ECDC. Since the reporting year 2002, 

outcome data are collected for all individual cases by 

submission of an individual dataset for the 12 months 

before the year for which notification data are reported 

to TESSy, and since 2008 also for MDR treatment outcome 

for cases reported 24 months before the year 

for which notification data are reported to TESSy. The 

cases eligible for outcome analysis (cohorts) include all 

the culture-confirmed pulmonary TB cases notified in 

the calendar year of interest, after exclusion of cases 

with final diagnosis other than TB. 

Country-specific data were extracted for 2007 for both 

new and retreatment laboratory-confirmed pulmonary 

TB cases for the analysis of 12 months of treatment 

outcome data. For 2006, country-specific data 

were extracted for laboratory-confirmed MDR TB cases 

(combined new and retreatment) for the analysis of 24 

months of treatment outcome data. Aggregated EU/ 

EEA data were extracted for the period 2003 to 2007 for 

trend analysis of treatment outcome for new, retreatment 

and combined laboratory-confirmed pulmonary 

Previously untreated Previously treated All Pulmonary cases 

2003 2004 2005 2006 2007 2003 2004 2005 2006 2007 2003 2004 2005 2006 2007 

16 www.eurosurveillance.org 

Year 

Transferred or unknown 

Still on treatment 

Defaulted 

Failed 

Died 

Success 

EEA: European Economic Area; EU: European Union. 

1 Excluding countries that did not or not in all years report cases: Austria, Bulgaria, Finland, France, Greece, Liechtenstein, Luxembourg, and 

Spain.

Table 1 

Treatment outcome in new and retreatment culture-confirmed pulmonary tuberculosis cases, by country, EU/EEA 

countries, 2007 (n=36,377) 


Cases notified 

in 2007 

Success Died Failed Defaulted 


Transferred or 

unknown 

Country 

New cases 

N N (%) N (%) N (%) N (%) N (%) N (%) 

Austria - - - - - - - - - - - - - 

Belgium1 499 342 (68.5) 42 (8.4) 0 (0.0) 44 (8.8) 12 (2.4) 59 (11.8) 

Bulgaria 1,233 972 (78.8) 85 (6.9) 4 (0.3) 96 (7.8) 41 (3.3) 35 (2.8) 

Cyprus - - - - - - - - - - - - - 

Czech Republic 459 331 (72.1) 86 (18.7) 4 (0.9) 32 (7.0) 4 (0.9) 2 (0.4) 

Denmark1 213 169 (79.3) 11 (5.2) 2 (0.9) 3 (1.4) 11 (5.2) 17 (8.0) 

Estonia 302 185 (61.3) 41 (13.6) 2 (0.7) 29 (9.6) 45 (14.9) 0 (0.0) 

Finland 181 126 (69.6) 35 (19.3) 1 (0.6) 2 (1.1) 7 (3.9) 10 (5.5) 

France - - - - - - - - - - - - - 

Germany 2,421 1,863 (77.0) 277 (11.4) 3 (0.1) 36 (1.5) 69 (2.9) 173 (7.1) 

Greece - - - - - - - - - - - - - 

Hungary 612 311 (50.8) 74 (12.1) 86 (14.1) 34 (5.6) 84 (13.7) 23 (3.8) 

Iceland 7 6 (85.7) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (14.3) 

Ireland1 181 127 (70.2) 10 (5.5) 0 (0.0) 3 (1.7) 8 (4.4) 33 (18.2) 

Italy - - - - - - - - - - - - - 

Latvia 772 634 (82.1) 54 (7.0) 1 (0.1) 32 (4.1) 51 (6.6) 0 (0.0) 

Liechtenstein - - - - - - - - - - - - - 

Lithuania 1,209 860 (71.1) 144 (11.9) 18 (1.5) 89 (7.4) 94 (7.8) 4 (0.3) 

Luxembourg - - - - - - - - - - - - - 

Malta 12 9 (75.0) 0 (0.0) 0 (0.0) 1 (8.3) 1 (8.3) 1 (8.3) 

Netherlands1 397 314 (79.1) 18 (4.5) 0 (0.0) 8 (2.0) 0 (0.0) 57 (14.4) 

Norway1 114 89 (78.1) 2 (1.8) 0 (0.0) 0 (0.0) 4 (3.5) 19 (16.7) 

Poland 4,502 3,444 (76.5) 269 (6.0) 12 (0.3) 448 (10.0) 16 (0.4) 313 (7.0) 

Portugal 1,694 1,467 (86.6) 90 (5.3) 5 (0.3) 52 (3.1) 56 (3.3) 24 (1.4) 

Romania 11,245 9,508 (84.6) 453 (4.0) 442 (3.9) 533 (4.7) 95 (0.8) 214 (1.9) 

Slovakia 304 260 (85.5) 36 (11.8) 1 (0.3) 5 (1.6) 1 (0.3) 1 (0.3) 

Slovenia 150 123 (82.0) 16 (10.7) 0 (0.0) 4 (2.7) 0 (0.0) 7 (4.7) 

Spain - - - - - - - - - - - - - 

Sweden1 237 157 (66.2) 17 (7.2) 0 (0.0) 2 (0.8) 8 (3.4) 53 (22.4) 

United Kingdom1 2,241 1,733 (77.3) 145 (6.5) 0 (0.0) 15 (0.7) 128 (5.7) 220 (9.8) 

Total New cases 

Retreatment cases 

28,985 23,030 (79.5) 1,905 (6.6) 581 (2.0) 1,468 (5.1) 735 (2.5) 1,266 (4.4) 

Austria - - - - - - - - - - - - - 

Belgium2 49 27 (55.1) 6 (12.2) 0 (0.0) 4 (8.2) 8 (16.3) 4 (8.2) 

Bulgaria 146 52 (35.6) 38 (26.0) 2 (1.4) 23 (15.8) 27 (18.5) 4 (2.7) 

Cyprus - - - - - - - - - - - - - 


Denmark2 18 8 (44.4) 3 (16.7) 0 (0.0) 1 (5.6) 1 (5.6) 5 (27.8) 

Estonia 66 31 (47.0) 5 (7.6) 3 (4.5) 13 (19.7) 14 (21.2) 0 (0.0) 

Finland 7 7 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 

France - - - - - - - - - - - - - 

Germany 178 114 (64.0) 25 (14.0) 3 (1.7) 8 (4.5) 13 (7.3) 15 (8.4) 

Greece - - - - - - - - - - - - - 

Hungary 130 51 (39.2) 26 (20.0) 26 (20.0) 12 (9.2) 13 (10.0) 2 (1.5) 

Iceland 1 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (100.0) 

Ireland2 28 16 (57.1) 4 (14.3) 0 (0.0) 0 (0.0) 3 (10.7) 5 (17.9) 

Italy - - - - - - - - - - - - - 

Latvia 167 96 (57.5) 14 (8.4) 2 (1.2) 17 (10.2) 36 (21.6) 2 (1.2) 


Lithuania 423 130 (30.7) 119 (28.1) 21 (5.0) 89 (21.0) 63 (14.9) 1 (0.2) 

17

Luxembourg - - - - - - - - - - - - - 

Malta 1 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (100.0) 

Netherlands 2 40 27 (67.5) 3 (7.5) 0 (0.0) 1 (2.5) 0 (0.0) 9 (22.5) 

Norway 2 17 13 (76.5) 1 (5.9) 0 (0.0) 0 (0.0) 1 (5.9) 2 (11.8) 

Poland 698 429 (61.5) 69 (9.9) 4 (0.6) 141 (20.2) 8 (1.1) 47 (6.7) 

Portugal 182 140 (76.9) 13 (7.1) 0 (0.0) 11 (6.0) 12 (6.6) 6 (3.3) 

Romania 4,933 2,462 (49.9) 479 (9.7) 683 (13.8) 767 (15.5) 325 (6.6) 217 (4.4) 

Slovakia 42 35 (83.3) 1 (2.4) 1 (2.4) 1 (2.4) 4 (9.5) 0 (0.0) 

Slovenia 13 10 (76.9) 3 (23.1) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 

Spain - - - - - - - - - - - - - 

Sweden 2 13 7 (53.8) 2 (15.4) 0 (0.0) 1 (7.7) 1 (7.7) 2 (15.4) 

United Kingdom 2 196 141 (71.9) 22 (11.2) 0 (0.0) 0 (0.0) 14 (7.1) 19 (9.7) 

Total retreatment 7,392 3,826 (51.8) 840 (11.4) 745 (10.1) 1,093 (14.8) 545 (7.4) 343 (4.6) 

Total for all 36,377 26,856 (73.8) 2,745 (7.5) 1,326 (3.6) 2,561 (7.0) 1,280 (3.5) 1,609 (4.4) 


1 Not previously diagnosed cases. 

2 Previously diagnosed cases. 

Table 2 

Treatment outcome in culture-confirmed pulmonary TB cases by geographic origin and by country, EU/EEA countries, 

2007 (n=37,160) 

Cases Success Died Failed Defaulted Still on treatment 


unknown 

Country 

National origin 

N N (%) N (%) N (%) N (%) N (%) N (%) 

Austria - - - - - - - - - - - - - 

Belgium 327 224 (68.5) 42 (12.8) 0 (0.0) 14 (4.3) 8 (2.4) 39 (11.9) 

Bulgaria 1,379 1,024 (74.2) 123 (8.9) 6 (0.4) 119 (8.6) 68 (4.9) 39 (2.8) 

Cyprus - - - - - - - - - - - - - 


Denmark1 113 89 (78.8) 10 (8.8) 1 (0.9) 1 (0.9) 4 (3.5) 8 (7.1) 

Estonia 312 184 (59.0) 38 (12.2) 3 (1.0) 36 (11.5) 51 (16.3) 0 (0.0) 

Finland 146 99 (67.8) 35 (24.0) 1 (0.7) 1 (0.7) 5 (3.4) 5 (3.4) 

France - - - - - - - - - - - - - 

Germany 1,680 1,214 (72.3) 292 (17.4) 6 (0.4) 28 (1.7) 47 (2.8) 93 (5.5) 

Greece - - - - - - - - - - - - - 

Hungary 719 345 (48.0) 100 (13.9) 113 (15.7) 43 (6.0) 94 (13.1) 24 (3.3) 

Iceland 1 1 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 

Ireland 149 103 (69.1) 14 (9.4) 0 (0.0) 3 (2.0) 2 (1.3) 27 (18.1) 

Italy - - - - - - - - - - - - - 

Latvia 887 691 (77.9) 66 (7.4) 3 (0.3) 44 (5.0) 82 (9.2) 1 (0.1) 


Lithuania 1,593 971 (61.0) 258 (16.2) 36 (2.3) 172 (10.8) 151 (9.5) 5 (0.3) 

Luxembourg - - - - - - - - - - - - - 

Malta 5 4 (80.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (20.0) 

Netherlands 198 148 (74.7) 19 (9.6) 0 (0.0) 6 (3.0) 0 (0.0) 25 (12.6) 

Norway 26 21 (80.8) 3 (11.5) 0 (0.0) 0 (0.0) 0 (0.0) 2 (7.7) 

Poland 5,178 3,863 (74.6) 338 (6.5) 16 (0.3) 586 (11.3) 24 (0.5) 351 (6.8) 

Portugal 1,622 1,397 (86.1) 93 (5.7) 5 (0.3) 48 (3.0) 56 (3.5) 23 (1.4) 

Romania 16,178 11,970 (74.0) 932 (5.8) 1,125 (7.0) 1,300 (8.0) 420 (2.6) 431 (2.7) 

Slovakia 346 296 (85.5) 38 (11.0) 2 (0.6) 6 (1.7) 4 (1.2) 0 (0.0) 

Slovenia 128 106 (82.8) 17 (13.3) 0 (0.0) 4 (3.1) 0 (0.0) 1 (0.8) 

Spain - - - - - - - - - - - - - 

Sweden 66 37 (56.1) 12 (18.2) 0 (0.0) 1 (1.5) 1 (1.5) 15 (22.7) 

United Kingdom 915 673 (73.6) 113 (12.3) 0 (0.0) 7 (0.8) 44 (4.8) 78 (8.5) 

Total Nationals 32,380 23,765 (73.4) 2,628 (8.1) 1,320 (4.1) 2,428 (7.5) 1,066 (3.3) 1,173 (3.6) 


Foreign origin 

Austria - - - - - - - - - - - - - 

Belgium 288 190 (66.0) 17 (5.9) 0 (0.0) 39 (13.5) 13 (4.5) 29 (10.1) 

Bulgaria 1 1 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 

Cyprus - - - - - - - - - - - - - 


Denmark 2 118 88 (74.6) 4 (3.4) 1 (0.8) 3 (2.5) 8 (6.8) 14 (11.9) 

Estonia 56 32 (57.1) 8 (14.3) 2 (3.6) 6 (10.7) 8 (14.3) 0 (0.0) 

Finland 42 34 (81.0) 0 (0.0) 0 (0.0) 1 (2.4) 2 (4.8) 5 (11.9) 

France - - - - - - - - - - - - - 

Germany 1,157 914 (79.0) 66 (5.7) 1 (0.1) 24 (2.1) 37 (3.2) 115 (9.9) 

Greece - - - - - - - - - - - - - 

Hungary 24 14 (58.3) 0 (0.0) 3 (12.5) 4 (16.7) 3 (12.5) 0 (0.0) 

Iceland 7 5 (71.4) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (28.6) 

Ireland 95 62 (65.3) 3 (3.2) 0 (0.0) 0 (0.0) 9 (9.5) 21 (22.1) 

Italy - - - - - - - - - - - - - 

Latvia 52 39 (75.0) 2 (3.8) 0 (0.0) 5 (9.6) 5 (9.6) 1 (1.9) 


Lithuania 43 21 (48.8) 7 (16.3) 3 (7.0) 6 (14.0) 6 (14.0) 0 (0.0) 

Luxembourg 18 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 18 (100.0) 

Malta 9 5 (55.6) 0 (0.0) 0 (0.0) 1 (11.1) 1 (11.1) 2 (22.2) 

Netherlands 285 216 (75.8) 10 (3.5) 0 (0.0) 4 (1.4) 0 (0.0) 55 (19.3) 

Norway 121 90 (74.4) 2 (1.7) 0 (0.0) 0 (0.0) 5 (4.1) 24 (19.8) 

Poland 22 10 (45.5) 0 (0.0) 0 (0.0) 3 (13.6) 0 (0.0) 9 (40.9) 

Portugal 249 208 (83.5) 8 (3.2) 0 (0.0) 15 (6.0) 12 (4.8) 6 (2.4) 

Romania 0 0 - 0 - 0 - 0 - 0 - 0 - 

Slovakia 4 2 (50.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (25.0) 1 (25.0) 

Slovenia 35 27 (77.1) 2 (5.7) 0 (0.0) 0 (0.0) 0 (0.0) 6 (17.1) 

Spain - - - - - - - - - - - - - 

Sweden 184 127 (69.0) 7 (3.8) 0 (0.0) 2 (1.1) 8 (4.3) 40 (21.7) 

United Kingdom 1,874 1,467 (78.3) 82 (4.4) 0 (0.0) 11 (0.6) 106 (5.7) 208 (11.1) 

Total Foreigners 4,780 3,607 (75.5) 227 (4.7) 11 (0.2) 151 (3.2) 225 (4.7) 559 (11.7) 


1 Excluding native cases < 26 years old whose parents were born outside Denmark 

2 Including native cases < 26 years old whose parents were born outside Denmark 

Figure 2 

Proportion of tuberculosis deaths by geographic origin, EU/EEA countries 1 , 2007 (of n=37,160 cases) 

Proportion of cases (%) 

30.0 

25.0 

20.0 

15.0 

10.0 

5.0 

0.0 

Belgium 

Nationals 

Foreigners 

Bulgaria 

Czech Republic 


Denmark 

Estonia 

Finland 

Germany 

Hungary 

Ireland 

Latvia 


1 Excluding countries that did not or not in all years report cases. 

Lithuania 

Luxembourg 

Netherlands 

Norway 

Poland 

Portugal 

Romania 

Slovakia 

Slovenia 

Sweden 


Total 

19

TB cases. The following case classification was used 

for the purpose of the analysis: 

• A laboratory-confirmed TB case was a patient with 

culture-confirmed disease due to Mycobacterium 

tuberculosis complex. 

• A new case was any case who had not received 

drug treatment for active TB in the past, or who 

received anti-TB drugs for less than one month. 

• A retreatment case was a case diagnosed with TB 

in the past and who received treatment with anti- 

TB drugs (excluding preventive therapy) for at least 

one month. 

• A pulmonary case was any case with TB affecting 

the lung parenchyma, the tracheo-bronchial tree or 

the larynx. 

• Multi-drug resistance was defined as resistance to 

at least isoniazid and rifampicin. 

• Foreign/national origin for comparison of treatment 

outcome by geographical origin of TB cases 

was classified according to place of birth: born in 

the country (national origin) or born outside the 

country (foreign origin). For countries reporting 

citizenship rather than place of birth, the former 

was used as a proxy of national/foreign origin. In 

Denmark, the place of birth of parents was also 

used to classify geographical origin. 

For the purpose of this analysis, internationally recommended 

outcome categories where used with two 

additional categories [9]: ‘still on treatment’ after 12 

months of treatment, and ‘unknown’. Adopted definitions 

in our study were: 

• Cured: The treatment has been completed and 

culture has become negative on samples taken at 

the end of treatment and on at least one previous 

occasion. 

• Completed: The treatment has been completed 

but the case does not meet the criteria for cure or 

treatment failure. 

• Failed: Culture or sputum smear remain positive or 

become positive again five months or later into the 

course of treatment. 

• Died: Death, irrespective of cause, occurred before 

the patient was cured or treatment was completed. 

• Defaulted: The treatment was interrupted for two 

months or more, not resulting from a decision of 

the care provider; or the patient was lost to followup 

for two months or more before the end of treatment, 

except if transferred. 

• Transferred: The patient was referred to another 

clinical unit for treatment, and information on outcome 

is not available. 

• Still on treatment: The patient is still on treatment 

at 12 (24 when applicable) months after the start 

of treatment and did not meet any other outcome 

during treatment. This category includes patients 

whose initial treatment was changed due to polyresistance 

(i.e. resistance to at least two first-line 

drugs) of the isolate taken at the start of treatment, 

whose treatment was prolonged because of side 

effects/complications, whose initial regimen had 

been planned for more than 12 months, or patients 

for whom information on the reasons for being still 

on treatment was not available. 

• Unknown: Information on outcome is not available, 

for cases not known to have been transferred. 

• Success: This refers to the combined number of 

patients belonging to the treatment categories 

‘cured’ and ‘completed’. The success rate target 

(established by the WHA as 85% of new smear-positive 

cases) has been adapted to the EU/EEA setting 

where bacteriological confirmation of cases 

is done by culture. Thus for the purposes of this 

study, a success rate target of 85% applies to new 

laboratory-confirmed cases. 

• Cohort: This includes all cases eligible for outcome 

analysis (cohorts); i.e. all the culture-confirmed 

pulmonary TB cases notified in the calendar year 

of interest, after exclusion of cases with final diagnosis 

other than TB. 

For the purpose of calculating the outcome variables, 

culture-confirmed pulmonary TB cases notified in the 

calendar year of interest were used as denominators. 

Data for one country were considered to be complete 

if the cohorts used as denominators included all culture-confirmed 

pulmonary TB cases notified in the 

year selected for analysis and if the combined total 

of ‘defaulted, transferred and unknown’ cases did not 

exceed 35% of cases notified in that year. 

Proportions of deaths by geographic origin were stratified 

by age to allow comparability. 

Adjustments to account for how countries with high 

numbers of cases influence the EU/EEA average were 

not performed as the study aimed at presenting overall 

figures for EU/EEA patients. 

Figure 3 

Age-stratified case fatality by geographic origin, EU/EEA 

countries, 2007 (of n=25,391 cases) 

0.0 

Age group (years) 

0-4 05-14 15-24 25-44 45-64 >64 

Nationals 1.6 1.2 0.7 6.0 7.6 19.7 


20 www.eurosurveillance.org 

Case fatality (%) 

25.0 

20.0 

15.0 

10.0 

5.0 

Nationals 

Foreign origin 

Foreign origin 8.3 0.0 0.1 2.4 6.8 16.9

Results 

Twenty-two countries reported TOM data at 12 months 

for culture-confirmed pulmonary TB cases reported 

in 2007. Data were considered to be complete as per 

study definition in all reporting countries. The overall 

treatment success rate for all laboratory-confirmed 

pulmonary cases was 73.8%. Of these patients, 7.5% 

died while being treated for TB, 3.6% failed treatment, 

7.0% defaulted, 3.5% were still on treatment at the end 

of the 12-month observation period and 4,4% had an 

outcome recorded as unknown or transferred (Figure 1, 

Table 1). 

Among new laboratory-confirmed pulmonary cases, 

79.5% had a successful outcome, 6.6% died, 2% failed, 

2.5% were still on treatment, and 4.4% were transferred 

or had an unknown outcome (Table 1). Among 

countries with more than 20 new culture-confirmed 

pulmonary cases, success rates varied widely from 

50.8% in Hungary to 86.6% and 85.5% in Portugal and 

Slovakia respectively. Three countries achieved treatment 

success in 85% or more of this category of cases: 

Iceland, 85.7%, Portugal, 86.6% and Slovakia, 85.5%. 

The percentage of cases that died while undergoing TB 

treatment ranged from 1.8% in Norway to 18.7% in the 

Czech Republic. Overall treatment success rates below 

75% were associated with a high loss to follow-up 

(defaulted and transferred or unknown) ranging from 

6.6% to 25.7%. 

Treatment outcomes for retreatment culture-confirmed 

pulmonary TB cases were reported from 22 EU/EEA 

Member States (Table 1). For seven countries, information 

about previous treatment was not distinguished 

and reported as previously diagnosed cases (Belgium, 

Denmark, Ireland, the Netherlands, Norway, Sweden 

and United Kingdom). Among these retreatment cases 

the overall success rate was lower (51.8%; range: 

0%–100%) than among new cases. Death (11.4%), 

treatment failure (10.1%), default (14.8%) and still on 

treatment (7.4%) were more frequently reported in 

this group than among new cases. Only six countries 

achieved a treatment success of at least 70% among 

retreatment cases (Table 1). 

Analysis of data by geographic origin revealed similar 

proportions of successfully treated cases of national 

origin (73.4%) and those of foreign origin (75.5%). 

However, marked differences were observed in the 

proportion of deaths, with higher percentages among 

cases of national origin (8.1%) compared with those of 

foreign origin (4.7%). Similarly, differences were found 

in the percentages of failed cases (4.1% in nationals 

versus 0.2% in cases of foreign origin) and transferred/ 

unknown (3.6% in nationals versus 11.7% in cases of 

foreign origin) (Table 2, Figure 2). 

With regards to the differences in proportion of deaths 

between foreign origin and national cases, the stratification 

of case fatality by age group (Figure 3) reveals 

that age acts as an effect modifier, where the proportion 

of deaths increased with increasing age. The 


highest case fatality was in the age group of over 

64-year-olds, regardless of geographical origin. The 

high case fatality in 0-4-year-old children in the group 

of foreign origin is a doubtful interpretation as there 

was only one death in this group. 

Fifteen countries (12 of which provided complete data 

as per study definition) reported the treatment outcome 

at 24 months for culture-confirmed MDR TB cases 

(new and retreatment). The overall treatment success 

in the 15 countries ranged from 19.8% to 100%. Of the 

entire cohort, 16.6% died while on treatment, 17.0% 

failed treatment and 13.2% defaulted. 17.0% of registered 

cases were still on treatment at the end of the 24 

months observation period and 5.3% had been transferred 

or had an unknown outcome (Table 3). 

Analysis of trends for the cohorts 2003 to 2007 did not 

reveal any significant difference in the proportions of 

cases belonging to any of the treatment outcome categories. 

Treatment success remained in the range of 

78% to 80% in the new laboratory-confirmed pulmonary 

cases. Minimal improvement from 48% to 52.2% 

was recorded between the 2006 and 2007 cohorts 

of retreatment culture-confirmed pulmonary cases 

(Figure 1). 

Discussion and conclusions 

This analysis of treatment outcome monitoring within 

the EU and EEA Member States revealed significant 

findings concerning TB control in the region. Firstly, it 

is a matter of concern that there has been only a marginal 

improvement in the number of countries reporting 

treatment outcomes to the EU-wide database, 

which increased by only one Member State compared 

with the 2006 cohort reporting (22 versus 21 countries). 

Similarly, the number of cases with an unknown 

treatment outcome because of transfer or ‘outcome 

unknown’, remained high with an average of 4.4% of 

all pulmonary culture-confirmed cases belonging to 

this category and with six of 22 countries reporting 

more than 10% of unknown outcomes. This represents 

a programmatic weakness in one of the pillars of TB 

control and highlights the importance of the monitoring 

and evaluation process [2,3,10]. 

More disturbing is the fact that there has been no significant 

improvement in the percentage of cases successfully 

treated over the past five years, with 79.5% of 

new laboratory-confirmed pulmonary cases successfully 

treated and 51.8% in retreatment cases. This is 

reflected at the level of the individual Member States: 

only three countries achieved the target of 85% success 

rate in 2007 compared with seven countries for 

the 2006 cohort. 

The authors would have wished to extend the analysis 

of completeness of treatment to all notified cases 

to gain further insight in the distribution and quality 

of outcomes; however data proved insufficient to pro- 

21

ceed with this approach since only few countries report 

treatment completion for all cases. 

Achieving high success rates becomes particularly 

important in a setting like the EU and EEA where the 

decline in incidence that was typical of the past few 

decades is becoming slower in most countries [2]. This 

trend is certainly influenced by many factors including 

importation of cases from high-burden countries, outbreaks 

among vulnerable populations, persisting MDR 

TB, and in some cases a lack of adequate TB control 

measures. In this setting it is essential to achieve optimal 

treatment success in all TB patients. 

The need for reaching the success rate target is justified 

by its potential epidemiological impact. Several epidemiological 

models have shown [11-14] that achieving 

the 85% success target coupled with a case detection 

of at least 70% would cause a decline in the annual TB 

incidence rate of 5-10% in the absence of co-infection 

with human immunodeficiency virus (HIV). These theoretical 

assumptions are further corroborated by empirical 

findings, particularly in the European context. In 

fact, the TB incidence has been declining rapidly all 

over Europe over the past century, but the decline has 

more than doubled following the introduction of effective 

treatment. 

The analysis of the data by geographical origin (national 

versus foreign) revealed a similarity in the two groups 

in terms of overall success rate. Differences exist in 

the distribution of negative outcomes with regard to 

geographic origin. However, stratifying case fatality 

by age showed that the excess proportion of deaths 

Table 3 

Treatment outcome of multidrug-resistant tuberculosis cases after 24 months of treatment, EU/EEA countries, 2006 cohort 

(n=1,190) 

Country 

Total number of 

MDR cases 

TOM after 24 months 

Success Died Failed Defaulted 



unknown 

N % N % N % N % N % N % 

Austria - - - - - - - - - - - - - 

Belgium 18 10 (55.6) 1 (5.6) 0 (0.0) 0 (0.0) 3 (16.7) 4 (22.2) 

Bulgaria - - - - - - - - - - - - - 

Cyprus 0 - - - - - - - - - - - - 


Denmark 3 2 (66.7) 0 (0.0) 0 (0.0) 0 (0.0) 1 (33.3) 0 (0.0) 

Estonia 53 24 (45.3) 12 (22.6) 2 (3.8) 14 (26.4) 1 (1.9) 0 (0.0) 

Finland - - - - - - - - - - - - - 

France - - - - - - - - - - - - - 

Germany 83 42 (50.6) 4 (4.8) 1 (1.2) 10 (12.0) 14 (16.9) 12 (14.5) 

Greece - - - - - - - - - - - - - 

Hungary 17 9 (52.9) 1 (5.9) 5 (29.4) 1 (5.9) 1 (5.9) 0 (0.0) 

Iceland 0 - - - - - - - - - - - - 

Ireland 4 1 (25.0) 0 (0.0) 0 (0.0) 1 (25.0) 0 (0.0) 2 (50.0) 

Italy - - - - - - - - - - - - - 

Latvia 142 87 (61.3) 34 (23.9) 6 (4.2) 15 (10.6) 0 (0.0) 0 (0.0) 


Lithuania - - - - - - - - - - - - - 

Luxembourg 0 - - - - - - - - - - - - 

Malta 2 2 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 

Netherlands - - - - - - - - - - - - - 

Norway 3 1 (33.3) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (66.7) 

Poland 32 11 (34.4) 4 (12.5) 3 (9.4) 4 (12.5) 0 (0.0) 10 (31.3) 

Portugal 25 16 (64.0) 6 (24.0) 1 (4.0) 2 (8.0) 0 (0.0) 0 (0.0) 

Romania 788 156 (19.8) 130 (16.5) 184 (23.4) 107 (13.6) 178 (22.6) 33 (4.2) 

Slovakia 7 3 (42.9) 2 (28.6) 0 (0.0) 0 (0.0) 2 (28.6) 0 (0.0) 

Slovenia 1 1 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 

Spain - - - - - - - - - - - - - 

Sweden - - - - - - - - - - - - - 

United Kingdom - - - - - - - - - - - - - 

Subtotal EU/EEA 1,190 368 (30.9) 198 (16.6) 202 (17.0) 157 (13.2) 202 (17.0) 63 (5.3) 

EEA: European Economic Area; EU: European Union; MDR: multidrug-resistant; TOM: treatment outcome monitoring. 


among nationals was attributed to older age. These 

findings are not unexpected, and the similarities in 

terms of success rate, evident also at country level, 

seem to suggest that foreign-born patients are not at a 

higher risk of unfavourable outcome. 

The analysis also revealed a potential for worsening of 

the M/XDR TB epidemic in the EU and EEA, resulting 

from the high default rates recorded among retreatment 

and MDR TB cases (14.8% and 13.2%, respectively). 

Despite the data limitations with respect to the 

MDR TB analysis (with regards to data representativeness 

completeness and quality assurance of laboratory 

methods) a clear need for strengthening case holding 

and treatment monitoring among these two populations 

(retreatment and MDR TB) emerges. As widely 

shown in the literature, defaulting and previous unsuccessful 

treatment represent the biggest risk factor for 

the emergence of drug resistance, in particular M/XDR 

TB [15-18]. 

The role that surveillance of TB treatment outcomes can 

and ought to play in strengthening TB control needs to 

be highlighted. Reporting of outcomes allows close 

monitoring of the ability of TB programmes to support 

and ensure completion of patients’ treatment. It also 

allows tailoring control activities to high-risk groups 

defined in terms of their inability to comply with treatment 

and achieve successful outcomes. 

The claim that an unknown or unreported treatment 

outcome does not necessarily represent a negative one 

should be balanced against the argument that lack of 

knowledge about treatment outcomes deprives the programme 

of essential information to guide TB control. 

Finally it should be noted that the importance of 

achieving the highest possible treatment success rate 

goes beyond its programmatic and epidemiological 

impact. Achieving universal success in treating individual 

patients remains a fundamental point in case 

management and patient care. 

The importance of treatment outcome monitoring needs 

to be further stressed and mechanisms explored to 

maximise progress towards achievement of the targets. 

Clinicians, public health experts and policy makers 

must be convinced of the importance of a standardised 

approach to monitoring of treatment including a proper 

evaluation of its implementation. Only by recognising 

the key position that treatment outcome monitoring 

holds in TB control can progress towards elimination 

be pursued. 

Acknowledgements 

The authors would like to acknowledge the work of the ECDC 

national surveillance focal points who make EU/EEA TB surveillance 

possible. Finally a sincere acknowledgment and 

thanks to all clinicians that recognise the importance of 

treatment outcome monitoring and who make its reporting 

possible. 


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23


Risk of developing tuberculosis from a school contact: 

retrospective cohort study, United Kingdom, 2009 

M Caley (michael.caley@benpct.nhs.uk) 1 , T Fowler 2 , S Welch 3 , A Wood 4 

1. Birmingham East and North Primary Care Trust, Birmingham, United Kingdom 

2. Heart of England Teaching Primary Care Trust, Birmingham, United Kingdom 

3. Heart of England Foundation Trust, Birmingham, United Kingdom 

4. Health Protection Unit West Midlands East, Birmingham, United Kingdom 


Caley M, Fowler T, Welch S, Wood A. Risk of developing tuberculosis from a school contact: retrospective cohort study, United Kingdom, 2009. Euro Surveill. 

2010;15(11):pii=19510. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19510 

To quantify the risk of developing tuberculosis (TB) 

following school contact with a student with smear 

positive respiratory TB in a population with a high 

background rate of tuberculosis, a retrospective 

cohort study was conducted. This study included all 

students and staff (n=1,065) at an inner city secondary 

school in Birmingham, United Kingdom (UK). Being 

in the same school year as the index case resulted 

in a significantly higher risk of being diagnosed with 

active TB (odds ratio (OR) 6.11) and either active or 

latent TB (OR 10.52) compared to the risk for pupils 

in other school years. Neither lower level classroom 

exposure in tutoring groups nor being a staff member 

resulted in significantly increased risk of infection. 

The number of cases detected in the school was significantly 

higher than compared with the TB notification 

rate for the respective age groups in the population in 

the area. This study is consistent with the small body 

of evidence that already exists suggesting that greater 

levels of classroom contact with a student with smear 

positive active TB significantly increases the risk of 

contracting active and latent TB. It also suggests that 

staff may be at a lower risk of active TB than students. 

It does not appear that being in an area with high TB 

incidence substantially alters the epidemiology of the 

outbreak or risk of transmission between students in 

comparison to other populations. 

Introduction 

Historically tuberculosis (TB) has been a major cause of 

premature death in the United Kingdom (UK). It remains 

a serious disease and active TB can lead to death if not 

treated. An outbreak of TB in a school often causes 

major concern for children and parents and generates 

significant volumes of work for health-care organisations. 

In these situations it is important that action is 

based on robust scientific evidence to ensure that the 

correct response is being applied. However, the current 

evidence base for the management of a school-based 

outbreak of TB is small and increasing the size of this 

will ensure that screening strategies are both safe and 

effective in identifying those with infection. 


The evidence base for the United Kingdom’s National 

Institute for Health and Clinical Excellence (NICE) recommendations 

for management of TB in schools [1] 

refers to five analytical studies [2-6] none of which are 

UK based, nor conducted in areas of high local prevalence 

of TB or where the majority of students are from 

black or minority ethnic (BME) groups. Of these studies 

only three have provided estimates of the relative risk 

to children and staff within the school following a case 

of smear positive (open) TB in a school pupil. 

We conducted a retrospective cohort study following a 

large school-based TB outbreak in a state funded secondary 

school in the inner city of Birmingham, UK. Over 

95% of the school’s students were from BME groups 

and all were aged 10-16 years. The school was located 

in an area of central Birmingham with a high proportion 

of residents from a BME group (68%) [7] and one 

of highest incidence rates of tuberculosis in England 

[8]. In 2006 and 2007 it had a direct standardised incidence 

rate for TB of 109.6 and 99.4 cases per 100,000 

population, respectively [9] compared with the UK 

average of 13.8 per 100,000 [10]. In both the 10-14 and 

15-19-year-old age groups in the school uptake area the 

TB incidence was 105.7 per 100,000 in 2007 [8]. 

The index case for the outbreak was a 16-year-old male 

who was diagnosed with smear positive respiratory TB 

in December 2008. He had been increasingly unwell 

with cough and weight loss since September 2008. He 

had attended the school as usual for the majority of 

this time after which he received antimicrobial therapy 

and became smear negative. Initially the students in 

the same school year as the index case were screened 

for TB in February 2009. As a result of this screening 

which yielded several secondary cases of active TB, 

the whole school population was offered screening 

as advised by national guidance [1]. Screening of the 

whole school was carried out in April 2009. 


This study aims to: 

• Identify the risks of developing tuberculosis following 

different types of school contact with a 

child with smear positive respiratory TB. 

• Quantify the magnitude of these risks. 

Methods 

Study population 

The study population comprised all students (886) 

and staff members (179) who attended or worked at 

the school between September 2008 and April 2009 

(n=1,065). The student population was evenly split 

between five school years (173-189 pupils in each 

year). Students in the same school year were all of a 

similar age. 

Outcome measures and case ascertainment 

The primary outcome measure was the diagnosis of 

active TB infection requiring full antimicrobial treatment 

by a physician specialising in infectious or respiratory 

diseases. The secondary outcome measure was 

the diagnosis of active or latent TB requiring chemoprophylaxis 

according to local TB screening protocols. 

Students were screened by Mantoux testing. All students 

with a positive Mantoux result (greater than 

15 mm if Bacillus Calmette-Guérin (BCG) vaccinated, 

Table 1 

Outcomes of tuberculosis exposure groups under study, United Kingdom, 2009 (n=1,065) 


greater than 5 mm if unvaccinated) were referred for 

further clinical assessment. All staff were over 18 years 

of age and were offered screening by chest radiograph 

or Mantoux testing if pregnant. All staff with an abnormal 

chest radiograph or a positive Mantoux result were 

referred for clinical assessment. 

All patients referred were assessed for TB infection 

by at least clinical history, clinical examination, chest 

radiograph and gamma interferon test (T-spot), plus 

microscopic examination of sputum if coughing. More 

invasive diagnostic testing was carried out as clinically 

indicated. Diagnosis of latent or active tuberculosis 

was made by a consultant respiratory physician. 

Measurement of exposure 

Data were collected for each subject during the coordinated 

health service response to the outbreak, 

including information on date of birth, address, history 

of BCG vaccination and for students, school year and 

tutoring group. 

Students from different school years did not mix for 

lessons but there was significant mixing of students 

within a school year for lessons. Class sizes varied 

from approximately 20-35 students. The only formal 

mixing of students between years was as part of a tutor 

Pupils Staff 

Same school year as 

index case 

Other school year Same tutor group as index case Other tutor group 

Active tuberculosis 12 0 7 5 0 12 

Latent tuberculosis 55 0 37 18 1 54 

No evidence of tuberculosis 698 172 103 595 15 683 

Did not attend screening 121 7 23 98 2 119 

Total 886 179 170 716 18 868 

Table 2 

Results of logistic regression analysis of exposure factors to the risk of being diagnosed with active or latent tuberculosis, 

United Kingdom, 2009 

Risk of being diagnosed with active tuberculosis 

Exposure Odds ratio 95% Confidence interval p-value 

Staff member (versus pupil) 0 0 0.99 

Male 0.89 0.28-2.84 0.85 

Previous BCG vaccination 2.83 0.36-22.09 0.32 

Same tutor group as index case 0 0 0.99 

Same school year as index case 6.11 1.91-19.48 0.002 

Risk of being diagnosed with active or latent tuberculosis 

Exposure Odds ratio 95% Confidence interval p-value 

Staff member (versus pupil) 0 0 0.99 

Male 1.12 0.68-1.85 0.66 

Previous BCG vaccination 1.32 0.68-2.58 0.41 

Same tutor group as index case 0.71 0.09-5.45 0.75 

Same school year as index case 10.52 6.14-18.03

group where a total of 18 students from different years 

shared a classroom weekly for 1.5 hours per week. 

For students, two measures of increased exposure 

were used; being in the same school year with the 

index case (three 30 hours of classroom exposure 

per week) and being in the same tutoring group (tutor 

groups included students from all school years, sharing 

a tutoring group equated to 1.5 hours classroom 

exposure per week). Students not in the same tutor 

group or school year were classified as having low 

school exposure (less than 1.5 hours per week). For 

staff substantial exposure was defined as those who 

had prolonged and direct contact with the index case. 

This exposure was assessed clinically by interview as 

part of a risk assessment for each staff member. 

Statistical analysis 

Standard descriptive statistics were used to summarise 

the data. The relationship between exposure 

and outcomes was analysed using logistic regression 

which allowed the effect of interactions between exposure 

categories on outcomes to be assessed. Reported 

p-values are all two-sided. Except where stated otherwise, 

the control group was all students classified 

as the low exposure group. Comparisons of risk 

were made with (i) those in the same school year as 

the index case, and (ii) those in the same tutor group 

as the index case and staff. The chi-square test was 

used to assess differences in the rate of TB infection 

between the school population and the overall rate 

seen in school uptake area population [8] All analysis 

was carried out using SPSS version 15. 

Results 

All students at the school were aged between 10 and 

16 years at the time of investigation, all of which were 

included in the study. The study also included all staff 

members employed at the school during the study 

period. 

All students and staff were offered screening. Staff 

numbered 179 and of these 172 participated (96.1%). 

There were 886 students and of these 765 (86.3%) participated. 

The remainder, 121 pupils and seven staff, 

declined screening. Complete data are available for 

all participants. The outcomes for the different groups 

under study are presented in Table 1. 

Being in the same school year as the index case 

resulted in a significantly higher risk of having active 

TB (OR 6.11) and either active or latent TB (OR 10.52) 

(Table 2). The lower level of classroom exposure of 

those attending the same tutoring groups did not 

result in any significantly increased risk. No staff member 

was diagnosed with active or latent TB. 

Previous BCG vaccination did not significantly reduce 

the risk of being diagnosed with active or latent TB. 

Multiple logistic regression analysis showed no significant 

interaction between exposure categories on 

outcomes. 

Applying the age specific rate of TB infection of the 

school uptake area population [8] to the school population 

it would be expected that there would be 0.94 

cases of TB diagnosed per year. This is significantly 

lower than the actual number seen in our outbreak 

investigation (chi-square p=0.002). 

Discussion 

The study supports current recommendations for management 

of TB cases in schools. The highest level of 

risk of being diagnosed with active or latent TB and 

therefore priority area of concern is children in the 

same school year as the index case. The increased 

level of exposure seen in other groups did not translate 

to substantially increased risk of infection. While 

we would not suggest that teachers with substantial 

levels of exposure should not be tested for TB in school 

based outbreaks, these results suggest they can be 

reassured they are unlikely to be at higher levels of risk 

for contracting active TB. 

It is possible that the high numbers of students diagnosed 

with active TB in our study were due to the 

high incidence rate in the population. However, the 

large and significant difference between the expected 

number of cases in the school and the number actually 

found makes it unlikely that the majority of 

cases detected by screening were due to previously 

undiagnosed TB acquired in the wider community. 

In addition, three cases with active TB had their 

Mycobacterium tuberculosis strains molecularly typed 

by DNA fingerprinting. All of them were indistinguishable 

from one another and identical to the strain found 

in the index case which strongly supports the school 

being the place of transmission. 

This study adds to the small evidence base related to 

school based TB outbreaks. A particular strength of 

the study is the size of the population, which is larger 

than most of the other published studies [2,3,6] and 

the relatively low proportion of the population that did 

not attend screening which increases the reliability of 

the results. 

The most significant limitation of this study is the sole 

use of chest radiograph in the screening of non-pregnant 

staff members. UK guidance recommends that this 

is satisfactory for those aged over 35 years and have 

had previous BCG vaccination [1]. However, those that 

do not satisfy these criteria should ideally be screened 

by Mantoux testing. Due to the limitation of the data 

available we were unable to estimate what proportion 

of staff should ideally have had Mantoux testing. 

Therefore caution should be used when interpreting 

the prevalence of latent TB in the staff population. 

However, the results for the prevalence of active TB in 

the staff group should still be reliable since all subjects 


had either normal chest radiographs or TB excluded by 

a physician if the radiograph was abnormal. 

Current NICE guidance quotes a relative risk for existing 

high school pupils compared to new school entrants of 

2.3 (95% CI 1.7-3.2) [3]. Only two other studies examined 

the risk of classroom versus non-classroom exposure 

(relative risk (RR) 2.3 95% CI 1.4-3.8) [2], (RR 10.9 

95% CI 8.7-13.4) [4]. We have reported OR because of 

the use of logistic regression and although not the 

same as RR their values become increasingly similar 

as the ratio of subjects without disease to those with 

disease increases above 6:1. This study’s main finding 

of the risk of students in the same school year 

developing active TB has a ratio of approximately 24:1. 

Therefore we can be confident that the values of the 

OR presented here can be directly compared to the RR 

reported in previous studies without the need for statistical 

correction. 

A number of other papers have discussed the epidemiology 

of school outbreaks but have not formally quantified 

risk. No studies were found that quantified the 

risk to staff of contracting TB from students although 

studies exist that examined risks to students taught by 

staff with open TB [11]. 

The results of this study are consistent with other studies 

published on school-based TB outbreaks and confirm 

that higher levels of classroom exposure to people 

with open TB significantly increase the risk of being 

diagnosed with active or latent TB. It also suggests 

that the risk to staff may be very small when teaching 

children who have open TB although more research is 

required to confirm this. It does not appear that being 

in an area of high background TB incidence substantially 

alters the epidemiology of the outbreak or risk of 

transmission between students in comparison to other 

populations and that there is no evidence that alternative 

screening strategies are required in this situation. 

References 

1. National Collaborating Centre for Chronic Conditions. 

Tuberculosis: clinical diagnosis and management of 

tuberculosis, and measures for its prevention and control. 

London (UK): Royal College of Physicians; 2006. Available 

from: http://www.guideline.gov/summary/summary. 

aspx?doc_id=8993&nbr=4877&ss=6&xl=999. 

2. Phillips L, Carlile J, Smith D. Epidemiology of a tuberculosis 

outbreak in a rural Missouri high school. Pediatrics 

2004;113(6):e514–9. 

3. Ridzon R, Kent JH, Valway S, Weismuller P, Maxwell R, Elcock 

M, et al. Outbreak of drug-resistant tuberculosis with secondgeneration 

transmission in a high school in California. J 

Pediatr. 1997;131(6):863–8. 

4. A school and community-based outbreak of Mycobacterium 

tuberculosis in northern Italy, 1992–3. The Lodi Tuberculosis 

Working Group. Epidemiol Infect. 1994;113(1):83–93. 

5. Rothman LM, Dubeski G. School contact tracing following a 

cluster of tuberculosis cases in two Scarborough schools. Can 

J Public Health. 1993;84(5):297–302. 

6. Sacks JJ, Brenner ER, Breeden DC, Anders HM, Parker RL. 

Epidemiology of a tuberculosis outbreak in a South Carolina 

junior high school. Am J Public Health. 1985;75(4):361–5. 


7. Office for National Statistics (ONS). [Internet]. Current 

Estimates - Population Estimates by Ethnic Group Mid-2007 for 

Primary Care Organisations (experimental). London: National 

Statistics. 2007. Available from: http://www.statistics.gov.uk/ 

StatBase/Product.asp?vlnk=14238. 

8. Health Protection Agency (HPA). [Internet]. Tuberculosis 

case reports by region, England, 1999-2008. London: Health 

Protection Agency, Available from: http://www.hpa.org.uk/ 

web/HPAweb&HPAwebStandard/HPAweb_C/1195733750930. 

9. Personal communication: West Midlands HPA Regional 

Epidemiology Unit. April 2009. 

10. Health Protection Agency (HPA). Tuberculosis case reports 

and rates by country, UK, 2008. London: Health Protection 

Agency. 2007. Available from: http://www.hpa.org.uk/web/ 

HPAweb&HPAwebStandard/HPAweb_C/1225268896252. 

11. Wales JM, Buchan AR, Cookson JB, Jones DA, Marshall BS. 

Tuberculosis in a primary school: the Uppingham outbreak. Br 

Med J (Clin Res Ed). 1985;291(6501):1039–40. 

27

National Notes 

Bulletins 


National Bulletins 


29




Austria 

Mitteilungen der Sanitätsverwaltung 

Bundesministerium für Gesundheit Familie und Jugend, Vienna. 

Monthly, print only. In German. 

http://www.bmgfj.gv.at/cms/site/thema.html?channel=CH0951 

Belgium 

Vlaams Infectieziektebulletin 

Department of Infectious Diseases Control, Flanders. 

Quarterly, print and online. In Dutch, summaries in English. 

http://www.infectieziektebulletin.be 

Bulletin d’information de la section d’Epidémiologie 

Institut Scientifique de la Santé Publique, Brussels 

Monthly, online. In French. 

http://www.iph.fgov.be/epidemio/epifr/episcoop/episcoop.htm 

Bulgaria 

Bulletin of the National Centre of Infectious and Parasitic Diseases, Sofia. 

Print version. In Bulgarian. 

http://www.ncipd.org/ 

Cyprus 

Newsletter of the Network for Surveillance and Control of Communicable 

Diseases in Cyprus 

Medical and Public Health Services, Ministry of Health, Nicosia 

Biannual, print and online. In Greek. 

http://www.moh.gov.cy 

Czech Republic 

Zpravy CEM (Bulletin of the Centre of 

Epidemiology and Microbiology) 

Centrum Epidemiologie a Mikrobiologie Státního 

Zdravotního Ústavu, Prague. 

Monthly, print and online. In Czech, titles in English. 

http://www.szu.cz/cema/adefaultt.htm 

EPIDAT (Notifications of infectious diseases in the Czech Republic) 

http://www.szu.cz/cema/epidat/epidat.htm 

Denmark 

EPI-NEWS 

Department of Epidemiology, Statens Serum Institut, Copenhagen. 

Weekly, print and online. In Danish and English. 

http://www.ssi.dk 

Finland 

Kansanterveys 

Department of Infectious Disease Epidemiology, National Public Health 

Institute, Helsinki. 

Monthly, print and online. In Finnish. 

http://www.ktl.fi/portal/suomi/julkaisut/kansanterveyslehti 

France 

Bulletin épidémiologique hebdomadaire 

Institut de veille sanitaire, Saint-Maurice Cedex. 

Weekly, print and online. In French. 

http://www.invs.sante.fr/beh/default.htm 

Germany 

Epidemiologisches Bulletin 

Robert Koch-Institut, Berlin 

Weekly, print and online. In German. 

http://www.rki.de/DE/Content/Infekt/EpidBull/epid__bull__node.html 


Hungary 

Epinfo (az Országos Epidemiológiai Központ epidemiológiai információs 

hetilapja) 

National Center For Epidemiology, Budapest. 

Weekly, online. In Hungarian. 

http://www.oek.hu/oek.web?to=839&nid=41&pid=7&lang=hun 

Iceland 

EPI-ICE 

Landlæknisembættið 

Directorate Of Health, Seltjarnarnes 

Monthly, online. In Icelandic and English. 

http://www.landlaeknir.is 

Ireland 

EPI-INSIGHT 

Health Protection Surveillance Centre, Dublin. 

Monthly, print and online. In English. 

http://www.ndsc.ie/hpsc/EPI-Insight 

Italy 

Notiziario dell’Istituto Superiore di Sanità 

Istituto Superiore di Sanità, Reparto di Malattie Infettive, Rome. 

Monthly, online. In Italian. 

http://www.iss.it/publ/noti/index.php?lang=1&tipo=4 

Bolletino Epidemiologico Nazionale (BEN) 

Istituto Superiore di Sanità, Reparto di Malattie Infettive, Rome. 

Monthly, online. In Italian. 

http://www.epicentro.iss.it/ben 

Latvia 

Epidemiologijas Bileteni 

Sabiedribas veselibas agentura 

Public Health Agency, Riga. 

Online. In Latvian. 

http://www.sva.lv/epidemiologija/bileteni 

Lithuania 

Epidemiologijos žinios 

Užkreciamuju ligu profilaktikos ir kontroles centras 

Center for Communicable Disease Prevention and Control, Vilnius. 

Online. In Lithuanian. 

http://www.ulac.lt/index.php?pl=26 

Netherlands 

Infectieziekten Bulletin 

Rijksinstituut voor Volksgezondheid en Milieu 

National Institute of Public Health and the Environment, Bilthoven 

Monthly, print and online. In Dutch. 

http://www.rivm.nl/infectieziektenbulletin 

Norway 

MSIS-rapport 

Folkehelseinstituttet, Oslo. 

Weekly, print and online. In Norwegian. 

http://www.folkehelsa.no/nyhetsbrev/msis 

Poland 

Meldunki o zachorowaniach na choroby zakazne i zatruciach w Polsce 

Panstwowy Zaklad Higieny, 

National Institute of Hygiene, Warsaw. 

Fortnightly, online. In Polish and English. 

http://www.pzh.gov.pl/epimeld/index_p.html#01 

31

Portugal 

Saúde em Números 

Ministério da Saúde, 

Direcção-Geral da Saúde, Lisbon. 

Sporadic, print only. In Portuguese. 

http://www.dgs.pt 

Romania 

Info Epidemiologia 

Centrul pentru Prevenirea si Controlul Bolilor Transmisibile, 

National Centre of Communicable Diseases Prevention and Control, Institute 

of Public Health, Bucharest. 

Sporadic, print only. In Romanian. 

http://www.cpcbt.ispb.ro 

Slovenia 

CNB Novice 

Inštitut za varovanje zdravja, Center za nalezljive bolezni, Institute of Public 

Health, Center for Infectious Diseases, Ljubljana. 

Monthly, online. In Slovene. 

http://www.ivz.si/index.php?akcija=podkategorija&p=89 

Spain 

Boletín Epidemiológico Semanal 

Centro Nacional de Epidemiología, Instituto de Salud Carlos III, Madrid. 

Fortnightly, print and online. In Spanish. 

http://www.isciii.es/jsps/centros/epidemiologia/boletinesSemanal.jsp 

Sweden 

EPI-aktuellt 

Smittskyddsinstitutet, Stockholm. 

Weekly, online. In Swedish. 

htpp://www.smittskyddsinstitutet.se/publikationer/smis-nyhetsbrev/epiaktuellt 


England and Wales 

Health Protection Report 

Health Protection Agency, London. 

Weekly, online only. In English. 

http://www.hpa.org.uk/hpr 

Northern Ireland 

Communicable Diseases Monthly Report 

Communicable Disease Surveillance Centre, Northern Ireland, Belfast. 

Monthly, print and online. In English. 

http://www.cdscni.org.uk/publications 

Scotland 

Health Protection Scotland Weekly Report 

Health Protection Scotland, Glasgow. 

Weekly, print and online. In English. 

http://www.hps.scot.nhs.uk/ewr/index.aspx 

Other journals 

EpiNorth journal 

Norwegian Institute of Public Health, Folkehelseinstituttet, Oslo, Norway 

Published four times a year in English and Russian. 

http://www.epinorth.org 

European Union 

“Europa” is the official portal of the European Union. It provides up-to-date 

coverage of main events and information on activities and institutions of the 

European Union. 

http://europa.eu 

European Commission - Public Health 

The website of European Commission Directorate General for Health and 

Consumer Protection (DG SANCO). 

http://ec.europa.eu/health/index_en.htm 

Health-EU Portal 

The Health-EU Portal (the official public health portal of the European Union) 

includes a wide range of information and data on health-related issues and 

activities at both European and international level. 

http://ec.europa.eu/health-eu/index_en.htm 


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